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Particle beam radiotherapy in the treatment of WHO grade 2 and 3 meningiomas: an early experience from Shanghai Proton and Heavy Ion Center

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Abstract

Purpose

To investigate the efficacy and safety of particle beam radiotherapy (PBRT) in the management of patients with WHO grade 2 and 3 meningiomas.

Methods

Thirty-six consecutive and non-selected patients with WHO grade 2 (n = 28) and grade 3 (n = 8) meningiomas were treated at the Shanghai Proton and Heavy Ion Center, from May 2015 to March 2022. The median age of the cohort at PBRT was 48 years. There were 25 and 11 patients treated with PBRT in the setting of newly diagnosed diseases and progressive/recurrent diseases, respectively. PBRT was utilized as re-irradiation in 5 patients. Proton radiotherapy (PRT) and carbon-ion radiotherapy (CIRT), with a median dose of 60 Gy-Equivalent (GyE), were provided to 30 and 6 patients, respectively.

Results

With a median follow-up of 23.3 months, the local control rates were 92.0%, 82.0%, and 82.0% at 1, 2, and 3 years for the entire cohort, respectively. Patients with WHO grade 2 meningiomas (100%, 94.1%, 94,1% at 1,2,3 years) had a much better local control than those with WHO grade 3 meningiomas (50%, 25%, 25% at 1,2,3 years; P < 0.001). Three patients, all with WHO grade 3 meningiomas, had deceased at the time of this analysis. Multivariate analyses revealed that WHO grade (grade 2 vs. 3) (p = 0.016) was a significant prognosticator for local control. No severe toxicities (G3 or above) were observed.

Conclusions

Treatment-induced efficacy and toxicities to PBRT in WHO grade 2 and 3 meningiomas were both highly acceptable. Longer follow-up is needed to evaluate the long-term outcome in terms of disease control, survival, as well as potential late effects.

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References

  1. Miller KD, Ostrom QT, Kruchko C, Patil N, Tihan T, Cioffi G, Fuchs HE, Waite KA, Jemal A, Siegel RL, Barnholtz-Sloan JS (2021) Brain and other central nervous system tumor statistics, 2021. Cancer J Clin 71:381–406. https://doi.org/10.3322/caac.21693

    Article  Google Scholar 

  2. Ostrom QT, Gittleman H, Xu J, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2016) CBTRUS Statistical Report: primary brain and other Central Nervous System Tumors diagnosed in the United States in 2009–2013. Neurooncology 18:v1–v75. https://doi.org/10.1093/neuonc/now207

    Article  Google Scholar 

  3. Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, Hawkins C, Ng HK, Pfister SM, Reifenberger G, Soffietti R, von Deimling A, Ellison DW (2021) The 2021 WHO classification of tumors of the Central Nervous System: a summary. Neurooncology 23:1231–1251. https://doi.org/10.1093/neuonc/noab106

    Article  CAS  Google Scholar 

  4. Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG 2nd (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64:56–60 discussion 60. https://doi.org/10.1227/01.NEU.0000330399.55586.63

  5. Sughrue ME, Sanai N, Shangari G, Parsa AT, Berger MS, McDermott MW (2010) Outcome and survival following primary and repeat surgery for World Health Organization Grade III meningiomas. J Neurosurg 113:202–209. https://doi.org/10.3171/2010.1.JNS091114

    Article  PubMed  Google Scholar 

  6. Coggins WS, Pham NK, Nguyen AV, Branch DW, Guillet JY, Korst G, Lall RR (2019) A systematic review of Ion Radiotherapy in maintaining local control regarding atypical and anaplastic meningiomas. World Neurosurg 132:282–291. https://doi.org/10.1016/j.wneu.2019.08.149

    Article  PubMed  Google Scholar 

  7. Bergner A, Maier AD, Mirian C, Mathiesen TI (2022) Adjuvant radiotherapy and stereotactic radiosurgery in grade 3 meningiomas - a systematic review and meta-analysis. Neurosurg Rev. https://doi.org/10.1007/s10143-022-01773-9

    Article  PubMed  Google Scholar 

  8. Hanft S, Canoll P, Bruce JN (2010) A review of malignant meningiomas: diagnosis, characteristics, and treatment. J Neurooncol 99:433–443. https://doi.org/10.1007/s11060-010-0348-9

    Article  CAS  PubMed  Google Scholar 

  9. Goldbrunner R, Stavrinou P, Jenkinson MD, Sahm F, Mawrin C, Weber DC, Preusser M, Minniti G, Lund-Johansen M, Lefranc F, Houdart E, Sallabanda K, Le Rhun E, Nieuwenhuizen D, Tabatabai G, Soffietti R, Weller M (2021) EANO guideline on the diagnosis and management of meningiomas. Neurooncology 23:1821–1834. https://doi.org/10.1093/neuonc/noab150

    Article  CAS  Google Scholar 

  10. Unterberger A, Nguyen T, Duong C, Kondajji A, Kulinich D, Yang I (2021) Meta-analysis of adjuvant radiotherapy for intracranial atypical and malignant meningiomas. J Neurooncol 152:205–216. https://doi.org/10.1007/s11060-020-03674-7

    Article  PubMed  Google Scholar 

  11. Brastianos PK, Galanis E, Butowski N, Chan JW, Dunn IF, Goldbrunner R, Herold-Mende C, Ippen FM, Mawrin C, McDermott MW, Sloan A, Snyder J, Tabatabai G, Tatagiba M, Tonn JC, Wen PY, Aldape K, Nassiri F, Zadeh G, Jenkinson MD, Raleigh DR, International Consortium on M (2019) Advances in multidisciplinary therapy for meningiomas. Neurooncology 21:i18–i31. https://doi.org/10.1093/neuonc/noy136

    Article  CAS  Google Scholar 

  12. Day SE, Halasz LM (2017) Radiation therapy for WHO grade I meningioma. Chin Clin Oncol 6:S4. https://doi.org/10.21037/cco.2017.06.01

    Article  PubMed  Google Scholar 

  13. Dennis ER, Bussiere MR, Niemierko A, Lu MW, Fullerton BC, Loeffler JS, Shih HA (2013) A comparison of critical structure dose and toxicity risks in patients with low grade gliomas treated with IMRT versus proton radiation therapy. Technol Cancer Res Treat 12:1–9. https://doi.org/10.7785/tcrt.2012.500276

    Article  CAS  PubMed  Google Scholar 

  14. Cozzi L, Fogliata A, Lomax A, Bolsi A (2001) A treatment planning comparison of 3D conformal therapy, intensity modulated photon therapy and proton therapy for treatment of advanced head and neck tumours. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology 61:287–297. https://doi.org/10.1016/s0167-8140(01)00403-0

    Article  CAS  PubMed  Google Scholar 

  15. Huang YW, Pan CY, Hsiao YY, Chao TC, Lee CC, Tung CJ (2015) Monte Carlo simulations of the relative biological effectiveness for DNA double strand breaks from 300 MeV u(-1) carbon-ion beams. Phys Med Biol 60:5995–6012. https://doi.org/10.1088/0031-9155/60/15/5995

    Article  CAS  PubMed  Google Scholar 

  16. Ando K, Kase Y (2009) Biological characteristics of carbon-ion therapy. Int J Radiat Biol 85:715–728. https://doi.org/10.1080/09553000903072470

    Article  CAS  PubMed  Google Scholar 

  17. Wu A, Jin MC, Meola A, Wong HN, Chang SD (2019) Efficacy and toxicity of particle radiotherapy in WHO grade II and grade III meningiomas: a systematic review. NeuroSurg Focus 46:E12. https://doi.org/10.3171/2019.3.FOCUS1967

    Article  PubMed  Google Scholar 

  18. Huang RY, Bi WL, Weller M, Kaley T, Blakeley J, Dunn I, Galanis E, Preusser M, McDermott M, Rogers L, Raizer J, Schiff D, Soffietti R, Tonn JC, Vogelbaum M, Weber D, Reardon DA, Wen PY (2019) Proposed response assessment and endpoints for meningioma clinical trials: report from the Response Assessment in Neuro-Oncology Working Group. Neurooncology 21:26–36. https://doi.org/10.1093/neuonc/noy137

    Article  CAS  Google Scholar 

  19. Kaley TJ, Wen P, Schiff D, Ligon K, Haidar S, Karimi S, Lassman AB, Nolan CP, DeAngelis LM, Gavrilovic I, Norden A, Drappatz J, Lee EQ, Purow B, Plotkin SR, Batchelor T, Abrey LE, Omuro A (2015) Phase II trial of sunitinib for recurrent and progressive atypical and anaplastic meningioma. Neurooncology 17:116–121. https://doi.org/10.1093/neuonc/nou148

    Article  CAS  Google Scholar 

  20. Lou E, Sumrall AL, Turner S, Peters KB, Desjardins A, Vredenburgh JJ, McLendon RE, Herndon JE 2nd, McSherry F, Norfleet J, Friedman HS, Reardon DA (2012) Bevacizumab therapy for adults with recurrent/progressive meningioma: a retrospective series. J Neurooncol 109:63–70. https://doi.org/10.1007/s11060-012-0861-0

  21. Nayak L, Iwamoto FM, Rudnick JD, Norden AD, Lee EQ, Drappatz J, Omuro A, Kaley TJ (2012) Atypical and anaplastic meningiomas treated with bevacizumab. J Neurooncol 109:187–193. https://doi.org/10.1007/s11060-012-0886-4

  22. Rydzewski NR, Lesniak MS, Chandler JP, Kalapurakal JA, Pollom E, Tate MC, Bloch O, Kruser T, Dalal P, Sachdev S (2018) Gross total resection and adjuvant radiotherapy most significant predictors of improved survival in patients with atypical meningioma. Cancer 124:734–742. https://doi.org/10.1002/cncr.31088

    Article  PubMed  Google Scholar 

  23. Kosaki K, Ecker S, Habermehl D, Rieken S, Jakel O, Herfarth K, Debus J, Combs SE (2012) Comparison of intensity modulated radiotherapy (IMRT) with intensity modulated particle therapy (IMPT) using fixed beams or an ion gantry for the treatment of patients with skull base meningiomas. Radiat Oncol 7:44. https://doi.org/10.1186/1748-717X-7-44

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ilicic K, Combs SE, Schmid TE (2018) New insights in the relative radiobiological effectiveness of proton irradiation. Radiat Oncol 13:6. https://doi.org/10.1186/s13014-018-0954-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. El Shafie RA, Czech M, Kessel KA, Habermehl D, Weber D, Rieken S, Bougatf N, Jakel O, Debus J, Combs SE (2018) Evaluation of particle radiotherapy for the re-irradiation of recurrent intracranial meningioma. Radiat Oncol 13:86. https://doi.org/10.1186/s13014-018-1026-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. El Shafie RA, Czech M, Kessel KA, Habermehl D, Weber D, Rieken S, Bougatf N, Jakel O, Debus J, Combs SE (2018) Clinical outcome after particle therapy for meningiomas of the skull base: toxicity and local control in patients treated with active rasterscanning. Radiat Oncol 13:54. https://doi.org/10.1186/s13014-018-1002-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Murray FR, Snider JW, Bolsi A, Lomax AJ, Walser M, Kliebsch U, Schneider RA, Weber DC (2017) Long-term clinical outcomes of Pencil Beam scanning Proton Therapy for Benign and Non-benign Intracranial Meningiomas. Int J Radiat Oncol Biol Phys 99:1190–1198. https://doi.org/10.1016/j.ijrobp.2017.08.005

    Article  PubMed  Google Scholar 

  28. Hansen TM, Bartlett GK, McMullen KP, McDonald MW (2015) Atypical and anaplastic Meningiomas: comparison of Outcomes between Photon and Proton Radiation Therapy. Int J Radiat Oncol Biol Phys 93:E61. https://doi.org/10.1016/j.ijrobp.2015.07.698

    Article  Google Scholar 

  29. McDonald MW, Plankenhorn DA, McMullen KP, Henderson MA, Dropcho EJ, Shah MV, Cohen-Gadol AA (2015) Proton therapy for atypical meningiomas. J Neurooncol 123:123–128. https://doi.org/10.1007/s11060-015-1770-9

    Article  CAS  PubMed  Google Scholar 

  30. Combs SE, Welzel T, Habermehl D, Rieken S, Dittmar JO, Kessel K, Jakel O, Haberkorn U, Debus J (2013) Prospective evaluation of early treatment outcome in patients with meningiomas treated with particle therapy based on target volume definition with MRI and 68Ga-DOTATOC-PET. Acta Oncol 52:514–520. https://doi.org/10.3109/0284186X.2013.762996

    Article  CAS  PubMed  Google Scholar 

  31. Combs SE, Kessel K, Habermehl D, Haberer T, Jakel O, Debus J (2013) Proton and carbon ion radiotherapy for primary brain tumors and tumors of the skull base. Acta Oncol 52:1504–1509. https://doi.org/10.3109/0284186X.2013.818255

    Article  PubMed  Google Scholar 

  32. Chan AW, Bernstein KD, Adams JA, Parambi RJ, Loeffler JS (2012) Dose escalation with proton radiation therapy for high-grade meningiomas. Technol Cancer Res Treat 11:607–614. https://doi.org/10.7785/tcrt.2012.500267

    Article  CAS  PubMed  Google Scholar 

  33. Weber DC, Schneider R, Goitein G, Koch T, Ares C, Geismar JH, Schertler A, Bolsi A, Hug EB (2012) Spot scanning-based proton therapy for intracranial meningioma: long-term results from the Paul Scherrer Institute. Int J Radiat Oncol Biol Phys 83:865–871. https://doi.org/10.1016/j.ijrobp.2011.08.027

    Article  PubMed  Google Scholar 

  34. Combs SE, Hartmann C, Nikoghosyan A, Jakel O, Karger CP, Haberer T, von Deimling A, Munter MW, Huber PE, Debus J, Schulz-Ertner D (2010) Carbon ion radiation therapy for high-risk meningiomas. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology 95:54–59. https://doi.org/10.1016/j.radonc.2009.12.029

    Article  CAS  PubMed  Google Scholar 

  35. Boskos C, Feuvret L, Noel G, Habrand JL, Pommier P, Alapetite C, Mammar H, Ferrand R, Boisserie G, Mazeron JJ (2009) Combined proton and photon conformal radiotherapy for intracranial atypical and malignant meningioma. Int J Radiat Oncol Biol Phys 75:399–406. https://doi.org/10.1016/j.ijrobp.2008.10.053

    Article  PubMed  Google Scholar 

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Funding

Shanghai Municipal Health Commission Special Clinical Research Project (Project No.20204Y0281, 202,040,295).

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Authors and Affiliations

  1. Shanghai Key Laboratory of Radiation Oncology (20dz2261000), Shanghai, China

    Xianxin Qiu, Jing Gao, Jiyi Hu, Jing Yang, Weixu Hu, Qingting Huang, Haojiong Zhang & Lin Kong

  2. Department of Radiation Oncology, Huashan Hospital, Fudan University, Shanghai, China

    Xianxin Qiu

  3. Department of Radiation Oncology, Shanghai Proton and Heavy Ion Center, Shanghai, China

    Jing Gao, Jiyi Hu, Jing Yang, Weixu Hu, Qingting Huang & Haojiong Zhang

  4. Shanghai Engineering Research Center of Proton and Heavy Ion Radiation Therapy, Shanghai, China

    Jing Gao, Jiyi Hu, Jing Yang, Weixu Hu, Qingting Huang, Haojiong Zhang & Lin Kong

  5. Proton and Heavy Ion Center, Heyou International Hospital, Tumor, Guangdong, China

    Jiade J. Lu

  6. Department of Radiation Oncology, Shanghai Proton and Heavy Ion Center, Fudan University Cancer Hospital, Shanghai, China

    Lin Kong

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  1. Xianxin Qiu
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Contributions

Conception and design: Lin Kong, Jiade J Lu. Acquisition of data: Xianxin Qiu, Jing Gao, Jiyi Hu, Jing Yang, Weixu Hu, Qingting Huang, Haojiong Zhang. Analysis and interpretation of data: Xianxin Qiu, Jing Gao. Drafting or revising the article: Xianxin Qiu, Lin Kong. All authors reviewed the manuscript.

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Correspondence to Lin Kong.

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Qiu, X., Gao, J., Hu, J. et al. Particle beam radiotherapy in the treatment of WHO grade 2 and 3 meningiomas: an early experience from Shanghai Proton and Heavy Ion Center. J Neurooncol 165, 241–250 (2023). https://doi.org/10.1007/s11060-023-04401-8

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