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J Neurol Surg A Cent Eur Neurosurg 2023; 84(02): 174-187
DOI: 10.1055/s-0042-1749351
Review Article

Updates in the Management of Recurrent Glioblastoma Multiforme

Hanuman Prasad Prajapati
1   Department of Neurosurgery, Uttar Pradesh University of Medical Sciences, Etawah, Uttar Pradesh, India
,
Ahmad Ansari
2   Department of Neurosurgery, Uttar Pradesh University of Medical Sciences, Safai, Uttar Pradesh, India
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Abstract

Background Glioblastoma is the most aggressive and diffusely infiltrative primary brain tumor. Recurrence is almost universal even after all primary standard treatments. This article aims to review the literature and update the standard treatment strategies for patients with recurrent glioblastoma.

Methods A systematic search was performed with the phrase “recurrent glioblastoma and management” as a search term in PubMed central, Medline, and Embase databases to identify all the articles published on the subject till December 2020. The review included peer-reviewed original articles, clinical trials, review articles, and keywords in title and abstract.

Results Out of 513 articles searched, 73 were included in this review after screening for eligibility. On analyzing the data, most of the studies report a median overall survival (OS) of 5.9 to 11.4 months after re-surgery and 4.7 to 7.6 months without re-surgery. Re-irradiation with stereotactic radiosurgery (SRS) and fractionated stereotactic radiotherapy (FSRT) result in a median OS of 10.2 months (range: 7.0–12 months) and 9.8 months (ranged: 7.5–11.0 months), respectively. Radiation necrosis was found in 16.6% (range: 0–24.4%) after SRS. Chemotherapeutic agents like nitrosourea (carmustine), bevacizumab, and temozolomide (TMZ) rechallenge result in a median OS in the range of 5.1 to 7.5, 6.5 to 9.2, and 5.1–13.0 months and six months progression free survival (PFS-6) in the range of 13 to 17.5%, 25 to 42.6%, and 23 to 58.3%, respectively. Use of epithelial growth factor receptor (EGFR) inhibitors results in a median OS in the range of 2.0 to 3.0 months and PFS-6 in 13%.

Conclusion Although recurrent glioblastoma remains a fatal disease with universal mortality, the literature suggests that a subset of patients may benefit from maximal treatment efforts.

Keywords

recurrent glioblastoma - management - outcomes - updates


Publication History

Received: 31 July 2021

Accepted: 03 March 2022

Article published online:
30 June 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Stupp R, Mason WP, van den Bent MJ. et al; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group.. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352 (10) 987-996
    CrossrefPubMedGoogle Scholar
  • 2 Stupp R, Taillibert S, Kanner A. et al. Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA 2017; 318 (23) 2306-2316
    CrossrefPubMedGoogle Scholar
  • 3 Petrecca K, Guiot MC, Panet-Raymond V, Souhami L. Failure pattern following complete resection plus radiotherapy and temozolomide is at the resection margin in patients with glioblastoma. J Neurooncol 2013; 111 (01) 19-23
    CrossrefPubMedGoogle Scholar
  • 4 Weller M, Cloughesy T, Perry JR, Wick W. Standards of care for treatment of recurrent glioblastoma: are we there yet?. Neuro-oncol 2013; 15 (01) 4-27
    CrossrefPubMedGoogle Scholar
  • 5 Patel M, Siddiqui F, Jin JY. et al. Salvage reirradiation for recurrent glioblastoma with radiosurgery: radiographic response and improved survival. J Neurooncol 2009; 92 (02) 185-191
    CrossrefPubMedGoogle Scholar
  • 6 Helseth R, Helseth E, Johannesen TB. et al. Overall survival, prognostic factors, and repeated surgery in a consecutive series of 516 patients with glioblastoma multiforme. Acta Neurol Scand 2010; 122 (03) 159-167
    CrossrefPubMedGoogle Scholar
  • 7 Tugcu B, Postalci LS, Gunaldi O, Tanriverdi O, Akdemir H. Efficacy of clinical prognostic factors on survival in patients with glioblastoma. Turk Neurosurg 2010; 20 (02) 117-125
    PubMedGoogle Scholar
  • 8 Rusthoven KE, Olsen C, Franklin W. et al. Favorable prognosis in patients with high-grade glioma with radiation necrosis: the University of Colorado reoperation series. Int J Radiat Oncol Biol Phys 2011; 81 (01) 211-217
    CrossrefPubMedGoogle Scholar
  • 9 Clark AJ, Lamborn KR, Butowski NA. et al. Neurosurgical management and prognosis of patients with glioblastoma that progresses during bevacizumab treatment. Neurosurgery 2012; 70 (02) 361-370
    CrossrefPubMedGoogle Scholar
  • 10 Park CK, Kim JH, Nam DH. et al. A practical scoring system to determine whether to proceed with surgical resection in recurrent glioblastoma. Neuro-oncol 2013; 15 (08) 1096-1101
    CrossrefPubMedGoogle Scholar
  • 11 McNamara MG, Lwin Z, Jiang H. et al. Factors impacting survival following second surgery in patients with glioblastoma in the temozolomide treatment era, incorporating neutrophil/lymphocyte ratio and time to first progression. J Neurooncol 2014; 117 (01) 147-152
    CrossrefPubMedGoogle Scholar
  • 12 Franceschi E, Bartolotti M, Tosoni A. et al. The effect of re-operation on survival in patients with recurrent glioblastoma. Anticancer Res 2015; 35 (03) 1743-1748
    PubMedGoogle Scholar
  • 13 Brandes AA, Bartolotti M, Tosoni A. et al. Patient outcomes following second surgery for recurrent glioblastoma. Future Oncol 2016; 12 (08) 1039-1044
    CrossrefPubMedGoogle Scholar
  • 14 Chen MW, Morsy AA, Liang S, Ng WH. Re-do craniotomy for recurrent grade IV glioblastomas: impact and outcomes from the National Neuroscience Institute Singapore. World Neurosurg 2016; 87: 439-445
    CrossrefPubMedGoogle Scholar
  • 15 Delgado-Fernandez J, Garcia-Pallero MÁ, Blasco G. et al. Usefulness of reintervention in recurrent glioblastoma: an indispensable weapon for increasing survival. World Neurosurg 2017; 108: 610-617
    CrossrefPubMedGoogle Scholar
  • 16 Zanello M, Roux A, Ursu R. et al; On the Behalf of the Club de Neuro-Oncologie of the Société Française de Neurochirurgie. Recurrent glioblastomas in the elderly after maximal first-line treatment: does preserved overall condition warrant a maximal second-line treatment?. J Neurooncol 2017; 135 (02) 285-297
    CrossrefPubMedGoogle Scholar
  • 17 Wann A, Tully PA, Barnes EH. et al. Outcomes after second surgery for recurrent glioblastoma: a retrospective case-control study. J Neurooncol 2018; 137 (02) 409-415
    CrossrefPubMedGoogle Scholar
  • 18 Kohshi K, Yamamoto H, Nakahara A, Katoh T, Takagi M. Fractionated stereotactic radiotherapy using gamma unit after hyperbaric oxygenation on recurrent high-grade gliomas. J Neurooncol 2007; 82 (03) 297-303
    CrossrefPubMedGoogle Scholar
  • 19 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 (05) 1742-1749
    CrossrefPubMedGoogle Scholar
  • 20 Fokas E, Wacker U, Gross MW, Henzel M, Encheva E, Engenhart-Cabillic R. Hypofractionated stereotactic reirradiation of recurrent glioblastomas : a beneficial treatment option after high-dose radiotherapy?. Strahlenther Onkol 2009; 185 (04) 235-240
    CrossrefPubMedGoogle Scholar
  • 21 Combs SE, Thilmann C, Edler L, Debus J, Schulz-Ertner D. Efficacy of fractionated stereotactic reirradiation in recurrent gliomas: long-term results in 172 patients treated in a single institution. J Clin Oncol 2005; 23 (34) 8863-8869
    CrossrefPubMedGoogle Scholar
  • 22 Laing RW, Warrington AP, Graham J, Britton J, Hines F, Brada M. Efficacy and toxicity of fractionated stereotactic radiotherapy in the treatment of recurrent gliomas (phase I/II study). Radiother Oncol 1993; 27 (01) 22-29
    CrossrefPubMedGoogle Scholar
  • 23 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 (02) 293-298
    CrossrefPubMedGoogle Scholar
  • 24 Fogh SE, Andrews DW, Glass J. et al. Hypofractionated stereotactic radiation therapy: an effective therapy for recurrent high-grade gliomas. J Clin Oncol 2010; 28 (18) 3048-3053
    CrossrefPubMedGoogle Scholar
  • 25 Kong D-S, Lee J-I, Park K, Kim JH, Lim DH, Nam DH. Efficacy of stereotactic radiosurgery as a salvage treatment for recurrent malignant gliomas. Cancer 2008; 112 (09) 2046-2051
    CrossrefPubMedGoogle Scholar
  • 26 Shrieve DC, Alexander III E, Wen PY. et al. Comparison of stereotactic radiosurgery and brachytherapy in the treatment of recurrent glioblastoma multiforme. Neurosurgery 1995; 36 (02) 275-282 , discussion 282–284
    CrossrefPubMedGoogle Scholar
  • 27 Combs SE, Widmer V, Thilmann C, Hof H, Debus J, Schulz-Ertner D. Stereotactic radiosurgery (SRS): treatment option for recurrent glioblastoma multiforme (GBM). Cancer 2005; 104 (10) 2168-2173
    CrossrefPubMedGoogle Scholar
  • 28 Pinzi V, Orsi C, Marchetti M. et al. Radiosurgery reirradiation for high-grade glioma recurrence: a retrospective analysis. Neurol Sci 2015; 36 (08) 1431-1440
    CrossrefPubMedGoogle Scholar
  • 29 Park KJ, Kano H, Iyer A. et al. Salvage gamma knife stereotactic radiosurgery followed by bevacizumab for recurrent glioblastoma multiforme: a case-control study. J Neurooncol 2012; 107 (02) 323-333
    CrossrefPubMedGoogle Scholar
  • 30 Cuneo KC, Vredenburgh JJ, Sampson JH. et al. Safety and efficacy of stereotactic radiosurgery and adjuvant bevacizumab in patients with recurrent malignant gliomas. Int J Radiat Oncol Biol Phys 2012; 82 (05) 2018-2024
    CrossrefPubMedGoogle Scholar
  • 31 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 (02) 337-345
    CrossrefPubMedGoogle Scholar
  • 32 Niyazi M, Ganswindt U, Schwarz SB. et al. Irradiation and bevacizumab in high-grade glioma retreatment settings. Int J Radiat Oncol Biol Phys 2012; 82 (01) 67-76
    CrossrefPubMedGoogle Scholar
  • 33 Conti A, Pontoriero A, Arpa D. et al. Efficacy and toxicity of CyberKnife re-irradiation and “dose dense” temozolomide for recurrent gliomas. Acta Neurochir (Wien) 2012; 154 (02) 203-209
    CrossrefPubMedGoogle Scholar
  • 34 Brandes AA, Tosoni A, Amistà P. et al. How effective is BCNU in recurrent glioblastoma in the modern era? A phase II trial. Neurology 2004; 63 (07) 1281-1284
    CrossrefPubMedGoogle Scholar
  • 35 van den Bent MJ, Brandes AA, Rampling R. et al. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J Clin Oncol 2009; 27 (08) 1268-1274
    CrossrefPubMedGoogle Scholar
  • 36 Reithmeier T, Graf E, Piroth T, Trippel M, Pinsker MO, Nikkhah G. BCNU for recurrent glioblastoma multiforme: efficacy, toxicity and prognostic factors. BMC Cancer 2010; 10: 30
    CrossrefPubMedGoogle Scholar
  • 37 Ahluwalia MS. 2010 Society for Neuro-Oncology Annual Meeting: a report of selected studies. Expert Rev Anticancer Ther 2011; 11 (02) 161-163
    CrossrefPubMedGoogle Scholar
  • 38 Batchelor T, Mulholland P, Neyns B. et al. The efficacy of cediranib as monotherapy and in combination with lomustine compared to lomustine alone in patients with recurrent glioblastoma: A phase III randomized trial. Neuro-oncol 2010; 12 (Suppl. 04) 75
    PubMedGoogle Scholar
  • 39 Scoccianti S, Detti B, Sardaro A. et al. Second-line chemotherapy with fotemustine in temozolomide-pretreated patients with relapsing glioblastoma: a single institution experience. Anticancer Drugs 2008; 19 (06) 613-620
    CrossrefPubMedGoogle Scholar
  • 40 Brandes AA, Tosoni A, Franceschi E. et al. Fotemustine as second-line treatment for recurrent or progressive glioblastoma after concomitant and/or adjuvant temozolomide: a phase II trial of Gruppo Italiano Cooperativo di Neuro-Oncologia (GICNO). Cancer Chemother Pharmacol 2009; 64 (04) 769-775
    CrossrefPubMedGoogle Scholar
  • 41 Fabrini MG, Silvano G, Lolli I. et al. A multi-institutional phase II study on second-line fotemustine chemotherapy in recurrent glioblastoma. J Neurooncol 2009; 92 (01) 79-86
    CrossrefPubMedGoogle Scholar
  • 42 Addeo R, Caraglia M, De Santi MS. et al. A new schedule of fotemustine in temozolomide-pretreated patients with relapsing glioblastoma. J Neurooncol 2011; 102 (03) 417-424
    CrossrefPubMedGoogle Scholar
  • 43 Kappelle AC, Postma TJ, Taphoorn MJ. et al. PCV chemotherapy for recurrent glioblastoma multiforme. Neurology 2001; 56 (01) 118-120
    CrossrefPubMedGoogle Scholar
  • 44 Schmidt F, Fischer J, Herrlinger U, Dietz K, Dichgans J, Weller M. PCV chemotherapy for recurrent glioblastoma. Neurology 2006; 66 (04) 587-589
    CrossrefPubMedGoogle Scholar
  • 45 Franceschi E, Omuro AM, Lassman AB, Demopoulos A, Nolan C, Abrey LE. Salvage temozolomide for prior temozolomide responders. Cancer 2005; 104 (11) 2473-2476
    CrossrefPubMedGoogle Scholar
  • 46 Kong DS, Lee JI, Kim WS. et al. A pilot study of metronomic temozolomide treatment in patients with recurrent temozolomide-refractory glioblastoma. Oncol Rep 2006; 16 (05) 1117-1121
    PubMedGoogle Scholar
  • 47 Berrocal A, Perez Segura P, Gil M. et al; GENOM Cooperative Group. Extended-schedule dose-dense temozolomide in refractory gliomas. J Neurooncol 2010; 96 (03) 417-422
    CrossrefPubMedGoogle Scholar
  • 48 Perry JR, Bélanger K, Mason WP. et al. Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J Clin Oncol 2010; 28 (12) 2051-2057
    CrossrefPubMedGoogle Scholar
  • 49 Kong DS, Lee JI, Kim JH. et al. Phase II trial of low-dose continuous (metronomic) treatment of temozolomide for recurrent glioblastoma. Neuro-oncol 2010; 12 (03) 289-296
    CrossrefPubMedGoogle Scholar
  • 50 Hammond A, Norden AD, Lesser GJ. et al. Phase II study of dose-intense temozolomide in recurrent glioblastoma. J Clin Oncol 2011; 29: 2038
    CrossrefPubMedGoogle Scholar
  • 51 Yung WK, Albright RE, Olson J. et al. A phase II study of temozolomide vs. procarbazine in patients with glioblastoma multiforme at first relapse. Br J Cancer 2000; 83 (05) 588-593
    CrossrefPubMedGoogle Scholar
  • 52 Stockhammer F, Misch M, Koch A. et al. Continuous low-dose temozolomide and celecoxib in recurrent glioblastoma. J Neurooncol 2010; 100 (03) 407-415
    CrossrefPubMedGoogle Scholar
  • 53 Quinn JA, Jiang SX, Reardon DA. et al. Phase II trial of temozolomide plus o6-benzylguanine in adults with recurrent, temozolomide-resistant malignant glioma. J Clin Oncol 2009; 27 (08) 1262-1267
    CrossrefPubMedGoogle Scholar
  • 54 Friedman HS, Prados MD, Wen PY. et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009; 27 (28) 4733-4740
    CrossrefPubMedGoogle Scholar
  • 55 Kreisl TN, Kim L, Moore K. et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 2009; 27 (05) 740-745
    CrossrefPubMedGoogle Scholar
  • 56 Raizer JJ, Grimm S, Chamberlain MC. et al. A phase 2 trial of single-agent bevacizumab given in an every-3-week schedule for patients with recurrent high-grade gliomas. Cancer 2010; 116 (22) 5297-5305
    CrossrefPubMedGoogle Scholar
  • 57 Chamberlain MC, Johnston SK. Salvage therapy with single agent bevacizumab for recurrent glioblastoma. J Neurooncol 2010; 96 (02) 259-269
    CrossrefPubMedGoogle Scholar
  • 58 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 (12) 1636-1640
    CrossrefPubMedGoogle Scholar
  • 59 Hasselbalch B, Lassen U, Hansen S. et al. Cetuximab, bevacizumab, and irinotecan for patients with primary glioblastoma and progression after radiation therapy and temozolomide: a phase II trial. Neuro-oncol 2010; 12 (05) 508-516
    PubMedGoogle Scholar
  • 60 Francesconi AB, Dupre S, Matos M. et al. Carboplatin and etoposide combined with bevacizumab for the treatment of recurrent glioblastoma multiforme. J Clin Neurosci 2010; 17 (08) 970-974
    CrossrefPubMedGoogle Scholar
  • 61 Reardon DA, Desjardins A, Peters KB. et al. Phase 2 study of carboplatin, irinotecan, and bevacizumab for recurrent glioblastoma after progression on bevacizumab therapy. Cancer 2011; 117 (23) 5351-5358
    CrossrefPubMedGoogle Scholar
  • 62 Sathornsumetee S, Desjardins A, Vredenburgh JJ. et al. Phase II trial of bevacizumab and erlotinib in patients with recurrent malignant glioma. Neuro-oncol 2010; 12 (12) 1300-1310
    CrossrefPubMedGoogle Scholar
  • 63 Taal W, Oosterkamp HM, Walenkamp AME. et al. A randomized phase ii study of bevacizumab versus bevacizumab plus lomustine versus lomustine single agent in recurrent glioblastoma: the Dutch belob study. J Clin Oncol 2013; 31 (15_suppl): 2001
    CrossrefPubMedGoogle Scholar
  • 64 Brandes A, Fichocchiaro G, Zagonel V. et al. Randomized phase ii trial AVAREG (ML25739) with bevacizumab (BEV) or fotemustine (FTM) in recurrent GBM: final results from the randomized phase ii trial. Ann Oncol 2014; 25 (Suppl. 04) iv137-iv145
    CrossrefPubMedGoogle Scholar
  • 65 de Groot JF, Lamborn KR, Chang SM. et al. Phase II study of aflibercept in recurrent malignant glioma: a North American Brain Tumor Consortium study. J Clin Oncol 2011; 29 (19) 2689-2695
    CrossrefPubMedGoogle Scholar
  • 66 Batchelor TT, Duda DG, di Tomaso E. et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J Clin Oncol 2010; 28 (17) 2817-2823
    CrossrefPubMedGoogle Scholar
  • 67 Yung WK, Vredenburgh JJ, Cloughesy TF. et al. Safety and efficacy of erlotinib in first-relapse glioblastoma: a phase II open-label study. Neuro-oncol 2010; 12 (10) 1061-1070
    CrossrefPubMedGoogle Scholar
  • 68 Raizer JJ, Abrey LE, Lassman AB. et al; North American Brain Tumor Consortium. A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro-oncol 2010; 12 (01) 95-103
    CrossrefPubMedGoogle Scholar
  • 69 Quant EC, Norden AD, Drappatz J. et al. Role of a second chemotherapy in recurrent malignant glioma patients who progress on bevacizumab. Neuro-oncol 2009; 11 (05) 550-555
    CrossrefPubMedGoogle Scholar
  • 70 Nguyen TD, Lassman AB, Lis E. et al. A pilot study to assess the tolerability and efficacy of RAD-001 (everolimus) with gefitinib in patients with recurrent glioblastoma multiforme(GBM). J Clin Oncol 2006; 24 (18) 1507
    CrossrefPubMedGoogle Scholar
  • 71 Doherty L, Gigas DC, Kesari S. et al. Pilot study of the combination of EGFR and mTOR inhibitors in recurrent malignant gliomas. Neurology 2006; 67 (01) 156-158
    CrossrefPubMedGoogle Scholar
  • 72 de Groot JF, Gilbert MR, Aldape K. et al. Phase II study of carboplatin and erlotinib (Tarceva, OSI-774) in patients with recurrent glioblastoma. J Neurooncol 2008; 90 (01) 89-97
    CrossrefPubMedGoogle Scholar
  • 73 Soffietti R, Trevisan E, Bertero L. et al. Bevacizumab and fotemustine for recurrent glioblastoma: a phase II study of AINO (Italian Association of Neuro-Oncology). J Neurooncol 2014; 116 (03) 533-541
    CrossrefPubMedGoogle Scholar
  • 74 Nieder C, Grosu AL, Molls M. A comparison of treatment results for recurrent malignant gliomas. Cancer Treat Rev 2000; 26 (06) 397-409
    CrossrefPubMedGoogle Scholar
  • 75 Ringel F, Pape H, Sabel M. et al; SN1 study group. Clinical benefit from resection of recurrent glioblastomas: results of a multicenter study including 503 patients with recurrent glioblastomas undergoing surgical resection. Neuro-oncol 2016; 18 (01) 96-104
    CrossrefPubMedGoogle Scholar
  • 76 Barbagallo GMV, Certo F, Di Gregorio S. et al. Recurrent high-grade glioma surgery: a multimodal intraoperative protocol to safely increase extent of tumor resection and analysis of its impact on patient outcome. Neurosurg Focus 2021; 50 (01) E20
    CrossrefPubMedGoogle Scholar
  • 77 Hoover JM, Nwojo M, Puffer R, Mandrekar J, Meyer FB, Parney IF. Surgical outcomes in recurrent glioma: clinical article. J Neurosurg 2013; 118 (06) 1224-1231
    CrossrefPubMedGoogle Scholar
  • 78 McGirt MJ, Chaichana KL, Gathinji M. et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 2009; 110 (01) 156-162
    CrossrefPubMedGoogle Scholar
  • 79 Montemurro N, Perrini P, Blanco MO, Vannozzi R. Second surgery for recurrent glioblastoma: a concise overview of the current literature. Clin Neurol Neurosurg 2016; 142: 60-64
    CrossrefPubMedGoogle Scholar
  • 80 Suchorska B, Weller M, Tabatabai G. et al. Complete resection of contrast-enhancing tumor volume is associated with improved survival in recurrent glioblastoma-results from the DIRECTOR trial. Neuro-oncol 2016; 18 (04) 549-556
    CrossrefPubMedGoogle Scholar
  • 81 Brem H, Piantadosi S, Burger PC. et al; The Polymer-brain Tumor Treatment Group. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. Lancet 1995; 345 (8956): 1008-1012
    CrossrefPubMedGoogle Scholar
  • 82 Metellus P, Coulibaly B, Nanni I. et al. Prognostic impact of O6-methylguanine-DNA methyltransferase silencing in patients with recurrent glioblastoma multiforme who undergo surgery and carmustine wafer implantation: a prospective patient cohort. Cancer 2009; 115 (20) 4783-4794
    CrossrefPubMedGoogle Scholar
  • 83 Xiao ZZ, Wang ZF, Lan T. et al. Carmustine as a supplementary therapeutic option for glioblastoma: a systematic review and meta-analysis. Front Neurol 2020; 11: 1036
    CrossrefPubMedGoogle Scholar
  • 84 Athanassiou H, Synodinou M, Maragoudakis E. et al. Randomized phase II study of temozolomide and radiotherapy compared with radiotherapy alone in newly diagnosed glioblastoma multiforme. J Clin Oncol 2005; 23 (10) 2372-2377
    CrossrefPubMedGoogle Scholar
  • 85 Barnett GH, Linskey ME, Adler JR. et al; American Association of Neurological Surgeons; Congress of Neurological Surgeons Washington Committee Stereotactic Radiosurgery Task Force. Stereotactic radiosurgery: an organized neurosurgery-sanctioned definition. J Neurosurg 2007; 106 (01) 1-5
    CrossrefPubMedGoogle Scholar
  • 86 Dincoglan F, Beyzadeoglu M, Sager O. et al. Management of patients with recurrent glioblastoma using hypofractionated stereotactic radiotherapy. Tumori 2015; 101 (02) 179-184
    CrossrefPubMedGoogle Scholar
  • 87 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 (04) 582-590
    CrossrefPubMedGoogle Scholar
  • 88 Cho KH, Hall WA, Gerbi BJ, Higgins PD, McGuire WA, Clark HB. Single dose versus fractionated stereotactic radiotherapy for recurrent high-grade gliomas. Int J Radiat Oncol Biol Phys 1999; 45 (05) 1133-1141
    CrossrefPubMedGoogle Scholar
  • 89 Sminia P, Mayer R. External beam radiotherapy of recurrent glioma: radiation tolerance of the human brain. Cancers (Basel) 2012; 4 (02) 379-399
    CrossrefPubMedGoogle Scholar
  • 90 Wang F, Zhou F, Kruh GD, Gallo JM. Influence of blood-brain barrier efflux pumps on the distribution of vincristine in brain and brain tumors. Neuro-oncol 2010; 12 (10) 1043-1049
    CrossrefPubMedGoogle Scholar
  • 91 Weller M, van den Bent M, Tonn JC. et al; European Association for Neuro-Oncology (EANO) Task Force on Gliomas. European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol 2017; 18 (06) e315-e329
    CrossrefPubMedGoogle Scholar
  • 92 Batchelor TT, Mulholland P, Neyns B. et al. Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J Clin Oncol 2013; 31 (26) 3212-3218
    CrossrefPubMedGoogle Scholar
  • 93 Blumenthal DT, Mendel L, Bokstein F. The optimal regimen of bevacizumab for recurrent glioblastoma: does dose matter?. J Neurooncol 2016; 127 (03) 493-502
    CrossrefPubMedGoogle Scholar
  • 94 Weller M, Tabatabai G, Reifenberger G. et al. Dose-intensified rechallenge with temozolomide: one week on/one week off versus 3 weeks on/one week off in patients with progressive or recurrent glioblastoma. J Clin Oncol 2010;28(15_suppl)
    PubMedGoogle Scholar
  • 95 Van Den Bent M, Eoli M, Sepulveda JM. et al. INTELLANCE 2/EORTC 1410 randomized phase II study of Depatux-M alone and with temozolomide vs temozolomide or lomustine in recurrent EGFR amplified glioblastoma. Neuro-oncol 2020; 22 (05) 684-693
    CrossrefPubMedGoogle Scholar
  • 96 Parrozzani R, Lombardi G, Midena E. et al. Ocular side effects of EGFR-inhibitor ABT-414 in recurrent glioblastoma: a long-term safety study. Front Oncol 2020; 10: 593461
    CrossrefPubMedGoogle Scholar
  • 97 Padovan M, Eoli M, Pellerino A. et al. Depatuxizumab Mafodotin (Depatux-M) plus temozolomide in recurrent glioblastoma patients: real-world experience from a multicenter study of Italian Association of Neuro-Oncology (AINO). Cancers (Basel) 2021; 13 (11) 2773
    CrossrefPubMedGoogle Scholar
  • 98 Omuro A, Vlahovic G, Lim M. et al. Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate 143. Neuro-oncol 2018; 20 (05) 674-686
    CrossrefPubMedGoogle Scholar
  • 99 Reardon DA, Brandes AA, Omuro A. et al. Effect of nivolumab vs bevacizumab in patients with recurrent glioblastoma: the CheckMate 143 phase 3 randomized clinical trial. JAMA Oncol 2020; 6 (07) 1003-1010
    CrossrefPubMedGoogle Scholar
  • 100 Ferris RL, Blumenschein Jr G, Fayette J. et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 2016; 375 (19) 1856-1867
    CrossrefPubMedGoogle Scholar
  • 101 Pitter KL, Tamagno I, Alikhanyan K. et al. Corticosteroids compromise survival in glioblastoma. Brain 2016; 139 (Pt 5): 1458-1471
    CrossrefPubMedGoogle Scholar
  • 102 Hegi ME, Diserens AC, Gorlia T. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352 (10) 997-1003
    CrossrefPubMedGoogle Scholar
  • 103 Borghaei H, Paz-Ares L, Horn L. et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 2015; 373 (17) 1627-1639
    CrossrefPubMedGoogle Scholar
  • 104 Wong ET, Lok E, Gautam S, Swanson KD. Dexamethasone exerts profound immunologic interference on treatment efficacy for recurrent glioblastoma. Br J Cancer 2015; 113 (02) 232-241
    CrossrefPubMedGoogle Scholar
  • 105 Birzu C, French P, Caccese M. et al. Recurrent glioblastoma: from molecular landscape to new treatment perspectives. Cancers (Basel) 2020; 13 (01) 47
    CrossrefPubMedGoogle Scholar
  • 106 Yao Y, Luo F, Tang C. et al. Molecular subgroups and B7-H4 expression levels predict responses to dendritic cell vaccines in glioblastoma: an exploratory randomized phase II clinical trial. Cancer Immunol Immunother 2018; 67 (11) 1777-1788
    CrossrefPubMedGoogle Scholar
  • 107 Markert JM, Medlock MD, Rabkin SD. et al. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 2000; 7 (10) 867-874
    CrossrefPubMedGoogle Scholar
  • 108 Kirson ED, Dbalý V, Tovarys F. et al. Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc Natl Acad Sci U S A 2007; 104 (24) 10152-10157
    CrossrefPubMedGoogle Scholar
  • 109 Kirson ED, Schneiderman RS, Dbalý V. et al. Chemotherapeutic treatment efficacy and sensitivity are increased by adjuvant alternating electric fields (TTFields). BMC Med Phys 2009; 9: 1
    CrossrefPubMedGoogle Scholar
  • 110 Stupp R, Wong ET, Kanner AA. et al. NovoTTF-100A versus physician's choice chemotherapy in recurrent glioblastoma: a randomised phase III trial of a novel treatment modality. Eur J Cancer 2012; 48 (14) 2192-2202
    CrossrefPubMedGoogle Scholar
  • 111 Cramer SW, Chen CC. Photodynamic therapy for the treatment of glioblastoma. Front Surg 2020; 6: 81
    CrossrefPubMedGoogle Scholar
  • 112 Giordano FA, Brehmer S, Mürle B. et al. Intraoperative radiotherapy in newly diagnosed glioblastoma (INTRAGO): an open-label, dose-escalation phase I/II trial. Neurosurgery 2019; 84 (01) 41-49
    CrossrefPubMedGoogle Scholar
  • 113 Mohammadi AM, Hawasli AH, Rodriguez A. et al. The role of laser interstitial thermal therapy in enhancing progression-free survival of difficult-to-access high-grade gliomas: a multicenter study. Cancer Med 2014; 3 (04) 971-979
    CrossrefPubMedGoogle Scholar
  • 114 Schwarzmaier H-J, Eickmeyer F, von Tempelhoff W. et al. MR-guided laser-induced interstitial thermotherapy of recurrent glioblastoma multiforme: preliminary results in 16 patients. Eur J Radiol 2006; 59 (02) 208-215
    CrossrefPubMedGoogle Scholar
  • 115 Slogan EA, Ahluwalia SM, Valerio-Pascua J. et al. Results of the NeuroBlate system first-in-humans Phase I Clinical trial for recurrent glioblastoma: clinical article. J Neurosurg 2013; 118 (06) 1202-1219
    CrossrefPubMedGoogle Scholar
  • 116 Bailly C, Vidal A, Bonnemaire C. et al. Potential for nuclear medicine therapy for glioblastoma treatment. Front Pharmacol 2019; 10: 772
    CrossrefPubMedGoogle Scholar
  • 117 Lim WA, June CH. The principles of engineering immune cells to treat cancer. Cell 2017; 168 (04) 724-740
    CrossrefPubMedGoogle Scholar
  • 118 Taslimi S, Ye VC, Wen PY, Zadeh G. Lessons learned from contemporary glioblastoma randomized clinical trials through systematic review and network meta-analysis: part 2 recurrent glioblastoma. Neurooncol Adv 2021; 3 (01) b029
    PubMedGoogle Scholar
  • 119 NCCN Clinical Practice Guidelines in Oncology. Central Nervous System Cancers. Version 1. 2015 Available at http://nccn.org/
    PubMedGoogle Scholar
  • 120 Ferguson M, Rodrigues G, Cao J, Bauman G. Management of high-grade gliomas in the elderly. Semin Radiat Oncol 2014; 24 (04) 279-288
    CrossrefPubMedGoogle Scholar
  • 121 Li J, Wang M, Won M. et al. Validation and simplification of the radiation therapy oncology group recursive partitioning analysis classification for glioblastoma. Int J Radiat Oncol Biol Phys 2011; 81 (03) 623-630
    CrossrefPubMedGoogle Scholar
  • 122 Kim HR, Kim KH, Kong DS. et al. Outcome of salvage treatment for recurrent glioblastoma. J Clin Neurosci 2015; 22 (03) 468-473
    CrossrefPubMedGoogle Scholar
  • 123 Quick J, Gessler F, Dützmann S. et al. Benefit of tumor resection for recurrent glioblastoma. J Neurooncol 2014; 117 (02) 365-372
    CrossrefPubMedGoogle Scholar
  • 124 Socha J, Kepka L, Ghosh S. et al. Outcome of treatment of recurrent glioblastoma multiforme in elderly and/or frail patients. J Neurooncol 2016; 126 (03) 493-498
    CrossrefPubMedGoogle Scholar
  • 125 Ranjan T, Howard CM, Yu A. et al. Cancer stem cell chemotherapeutics assay for prospective treatment of recurrent glioblastoma and progressive anaplastic glioma: a single-institution case series. Transl Oncol 2020; 13 (04) 100755
    CrossrefPubMedGoogle Scholar