Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Current Oncology Reports
Published in: Current Oncology Reports 5/2024

28-03-2024 | Glioblastoma | REVIEW

Novel Clinical Trials and Approaches in the Management of Glioblastoma

Authors: Allison R. Valerius, Lauren M. Webb, Ugur Sener

Published in: Current Oncology Reports | Issue 5/2024

Login to get access

Abstract

Purpose of Review

The purpose of this review is to discuss a wide variety of novel therapies recently studied or actively undergoing study in patients with glioblastoma. This review also discusses current and future strategies for improving clinical trial design in patients with glioblastoma to maximize efficacy in discovering effective treatments.

Recent Findings

Over the years, there has been significant expansion in therapy modalities studied in patients with glioblastoma. These therapies include, but are not limited to, targeted molecular therapies, DNA repair pathway targeted therapies, immunotherapies, vaccine therapies, and surgically targeted radiotherapies.

Summary

Glioblastoma is the most common malignant primary brain tumor in adults and unfortunately remains with poor overall survival following the current standard of care. Given the dismal prognosis, significant clinical and research efforts are ongoing with the goal of improving patient outcomes and enhancing quality and quantity of life utilizing a wide variety of novel therapies.
Literature
1.
Ostrom QT, Price M, Neff C, Cioffi G, Waite KA, Kruchko C, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2016–2020. Neuro Oncol. 2023;25(Supplement_4):iv1-iv99
2.
Ostrom QT, Price M, Neff C, Cioffi G, Waite KA, Kruchko C, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2015–2019. Neuro Oncol. 2022;24(Suppl 5):v1–95.PubMedPubMedCentralCrossRef
3.
Leece R, Xu J, Ostrom QT, Chen Y, Kruchko C, Barnholtz-Sloan JS. Global incidence of malignant brain and other central nervous system tumors by histology, 2003–2007. Neuro Oncol. 2017;19(11):1553–64.PubMedPubMedCentralCrossRef
4.
•• PY Wen M Weller EQ Lee BM Alexander JS Barnholtz-Sloan FP Barthel et al 2020 Glioblastoma in adults: a Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions Neuro Oncol 22 8 1073 1113. This paper published in 2020 provides an excellent review of the current management and future directions of glioblastoma at the time of publication. Topics including standar therapy, surgical management, radiotherapy, various chemotherapies, and many novel therapies are discussed. Novel therapies at the time included targeted molecular therapies, DNA damage response therapies, tumor metabolism targeting therapies, immunotherapies, and viral therapies. The paper also discusses potential improvements in clinical trial design.
5.
Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.PubMedCrossRef
6.
Hovey EJ, Field KM, Rosenthal MA, Barnes EH, Cher L, Nowak AK, et al. Continuing or ceasing bevacizumab beyond progression in recurrent glioblastoma: an exploratory randomized phase II trial. Neurooncol Pract. 2017;4(3):171–81.PubMedPubMedCentral
7.
Perry JR, Bélanger K, Mason WP, Fulton D, Kavan P, Easaw J, et al. Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J Clin Oncol. 2010;28(12):2051–7.PubMedCrossRef
8.
Wick W, Gorlia T, Bendszus M, Taphoorn M, Sahm F, Harting I, et al. Lomustine and bevacizumab in progressive glioblastoma. N Engl J Med. 2017;377(20):1954–63.PubMedCrossRef
9.
Shi W, Scannell Bryan M, Gilbert MR, Mehta MP, Blumenthal DT, Brown PD, 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(1):38–44.PubMedCrossRef
10.
Nabors LB, Portnow J, Ahluwalia M, Baehring J, Brem H, Brem S, et al. Central nervous system cancers, version 3.2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2020;18(11):1537–70.PubMedCrossRef
11.
Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216):1061–8.
12.
13.
Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98–110.PubMedPubMedCentralCrossRef
14.
Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, et al. The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol. 2021;23(8):1231–51.PubMedPubMedCentralCrossRef
15.
Wang J, Cazzato E, Ladewig E, Frattini V, Rosenbloom DI, Zairis S, et al. Clonal evolution of glioblastoma under therapy. Nat Genet. 2016;48(7):768–76.PubMedPubMedCentralCrossRef
16.
Ceccarelli M, Barthel FP, Malta TM, Sabedot TS, Salama SR, Murray BA, et al. Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse glioma. Cell. 2016;164(3):550–63.PubMedPubMedCentralCrossRef
17.
Le Rhun E, Preusser M, Roth P, Reardon DA, van den Bent M, Wen P, et al. Molecular targeted therapy of glioblastoma. Cancer Treat Rev. 2019;80:101896.PubMedCrossRef
18.
Ohgaki H, Kleihues P. The definition of primary and secondary glioblastoma. Clin Cancer Res. 2013;19(4):764–72.PubMedCrossRef
19.
Nishikawa R, Ji XD, Harmon RC, Lazar CS, Gill GN, Cavenee WK, et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc Natl Acad Sci U S A. 1994;91(16):7727–31.PubMedPubMedCentralCrossRef
20.
Weller M, Butowski N, Tran DD, Recht LD, Lim M, Hirte H, et al. Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncol. 2017;18(10):1373–85.PubMedCrossRef
21.
van den Bent M, Gan HK, Lassman AB, Kumthekar P, Merrell R, Butowski N, et al. Efficacy of depatuxizumab mafodotin (ABT-414) monotherapy in patients with EGFR-amplified, recurrent glioblastoma: results from a multi-center, international study. Cancer Chemother Pharmacol. 2017;80(6):1209–17.PubMedPubMedCentralCrossRef
22.
Van Den Bent M, Eoli M, Sepulveda JM, Smits M, Walenkamp A, Frenel JS, 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(5):684–93.PubMedCrossRef
23.
Reardon DA, Lassman AB, van den Bent M, Kumthekar P, Merrell R, Scott AM, et al. Efficacy and safety results of ABT-414 in combination with radiation and temozolomide in newly diagnosed glioblastoma. Neuro Oncol. 2017;19(7):965–75.PubMed
24.
Lim Y, Yoo J, Kim MS, Hur M, Lee EH, Hur HS, et al. GC1118, an anti-EGFR antibody with a distinct binding epitope and superior inhibitory activity against high-affinity EGFR ligands. Mol Cancer Ther. 2016;15(2):251–63.PubMedCrossRef
25.
Choi SW, Jung HA, Cho HJ, Kim TM, Park CK, Nam DH, et al. A multicenter, phase II trial of GC1118, a novel anti-EGFR antibody, for recurrent glioblastoma patients with EGFR amplification. Cancer Med. 2023;12(15):15788–96.PubMedPubMedCentralCrossRef
26.
Raizer JJ, Abrey LE, Lassman AB, Chang SM, Lamborn KR, Kuhn JG, et al. A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro Oncol. 2010;12(1):95–103.PubMedCrossRef
27.
Doherty L, Gigas DC, Kesari S, Drappatz J, Kim R, Zimmerman J, et al. Pilot study of the combination of EGFR and mTOR inhibitors in recurrent malignant gliomas. Neurology. 2006;67(1):156–8.PubMedCrossRef
28.
Froelich W. A new drug targeting EGFR in glioblastoma tumors. Oncology Times. 2021;43(24):21–2.CrossRef
29.
Kizilbash SH, Jaeckle KA, Mrugala MM, Allred JB, Safgren SL, Lammers AA, et al. First-in-human phase 1 trial of the safety, tolerability, pharmacokinetics, and preliminary anti-tumor activity of WSD0922-Fu: initial report from dose escalation cohort. J Clin Oncol. 2023;41(16_suppl):3109-.
30.
Nakajima N, Nobusawa S, Nakata S, Nakada M, Yamazaki T, Matsumura N, et al. BRAF V600E, TERT promoter mutations and CDKN2A/B homozygous deletions are frequent in epithelioid glioblastomas: a histological and molecular analysis focusing on intratumoral heterogeneity. Brain Pathol. 2018;28(5):663–73.PubMedCrossRef
31.
Kleinschmidt-DeMasters BK, Aisner DL, Birks DK, Foreman NK. Epithelioid GBMs show a high percentage of BRAF V600E mutation. Am J Surg Pathol. 2013;37(5):685–98.PubMedPubMedCentralCrossRef
32.
Kaley T, Touat M, Subbiah V, Hollebecque A, Rodon J, Lockhart AC, et al. BRAF inhibition in BRAF(V600)-mutant gliomas: results from the VE-BASKET study. J Clin Oncol. 2018;36(35):3477–84.PubMedPubMedCentralCrossRef
33.
Schreck K, Strowd R, Nabors LB, Ellingson B, Fisher J, Desideri S, et al. CTNI-60. Preliminary results of binimetinib and encorafenib in adults with recurrent BRAF V600E-mutated high-grade glioma. Neuro Oncol 2022;24(Supplement_7):vii86-vii
34.
Bouffet E, Hansford JR, Garrè ML, Hara J, Plant-Fox A, Aerts I, et al. Dabrafenib plus trametinib in pediatric glioma with BRAF V600 mutations. N Engl J Med. 2023;389(12):1108–20.PubMedCrossRef
35.
Wen PY, Stein A, van den Bent M, De Greve J, Wick A, de Vos F, et al. Dabrafenib plus trametinib in patients with BRAF(V600E)-mutant low-grade and high-grade glioma (ROAR): a multicentre, open-label, single-arm, phase 2, basket trial. Lancet Oncol. 2022;23(1):53–64.PubMedCrossRef
36.
Winstead E. Dabrafenib–trametinib combination approved for solid tumors with BRAF mutations [internet]. National Cancer Institute Cancer Currents Blog 2022
37.
Chen C, Zhu S, Zhang X, Zhou T, Gu J, Xu Y, et al. Targeting the synthetic vulnerability of PTEN-deficient glioblastoma cells with MCL1 inhibitors. Mol Cancer Ther. 2020;19(10):2001–11.PubMedCrossRef
38.
Galanis E, Buckner JC, Maurer MJ, Kreisberg JI, Ballman K, Boni J, et al. Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: a North Central Cancer Treatment Group Study. J Clin Oncol. 2005;23(23):5294–304.PubMedCrossRef
39.
Chang SM, Wen P, Cloughesy T, Greenberg H, Schiff D, Conrad C, et al. Phase II study of CCI-779 in patients with recurrent glioblastoma multiforme. Invest New Drugs. 2005;23(4):357–61.PubMedCrossRef
40.
Ma DJ, Galanis E, Anderson SK, Schiff D, Kaufmann TJ, Peller PJ, et al. A phase II trial of everolimus, temozolomide, and radiotherapy in patients with newly diagnosed glioblastoma: NCCTG N057K. Neuro Oncol. 2014;17(9):1261–9.PubMedPubMedCentralCrossRef
41.
Wick W, Gorlia T, Bady P, Platten M, van den Bent MJ, Taphoorn MJB, et al. Phase II study of radiotherapy and temsirolimus versus radiochemotherapy with temozolomide in patients with newly diagnosed glioblastoma without MGMT promoter hypermethylation (EORTC 26082). Clin Cancer Res. 2016;22(19):4797–806.PubMedCrossRef
42.
Wen PY, Groot JFd, Battiste J, Goldlust SA, Garner JS, Friend J, et al. Paxalisib in patients with newly diagnosed glioblastoma with unmethylated MGMT promoter status: final phase 2 study results. J Clin Oncol. 2022;40(16_suppl):2047-
43.
44.
45.
46.
Gousias K, Theocharous T, Simon M. Mechanisms of cell cycle arrest and apoptosis in glioblastoma. Biomedicines. 2022;10(3):564
47.
Taylor JW, Parikh M, Phillips JJ, James CD, Molinaro AM, Butowski NA, et al. Phase-2 trial of palbociclib in adult patients with recurrent RB1-positive glioblastoma. J Neurooncol. 2018;140(2):477–83.PubMedPubMedCentralCrossRef
48.
Lee EQ, Trippa L, Fell G, Rahman R, Arrillaga-Romany I, Touat M, et al. Preliminary results of the abemaciclib arm in the Individualized Screening Trial of Innovative Glioblastoma Therapy (INSIGhT): a phase II platform trial using Bayesian adaptive randomization. J Clin Oncol 2021;39(15_suppl):2014-
49.
Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, 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(5):740–5.PubMedCrossRef
50.
Cohen MH, Shen YL, Keegan P, Pazdur R. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist. 2009;14(11):1131–8.PubMedCrossRef
51.
Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):699–708.PubMedPubMedCentralCrossRef
52.
Sandmann T, Bourgon R, Garcia J, Li C, Cloughesy T, Chinot OL, et al. Patients with proneural glioblastoma may derive overall survival benefit from the addition of bevacizumab to first-line radiotherapy and temozolomide: retrospective analysis of the AVAglio trial. J Clin Oncol. 2015;33(25):2735–44.PubMedPubMedCentralCrossRef
53.
Batchelor TT, Mulholland P, Neyns B, Nabors LB, Campone M, Wick A, 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):3212–8.PubMedPubMedCentralCrossRef
54.
Lombardi G, De Salvo GL, Brandes AA, Eoli M, Rudà R, Faedi M, et al. Regorafenib compared with lomustine in patients with relapsed glioblastoma (REGOMA): a multicentre, open-label, randomised, controlled, phase 2 trial. Lancet Oncol. 2019;20(1):110–9.PubMedCrossRef
55.
•• Wen P, Alexander B, Berry D, Buxton M, Cavenee W, Colman H, et al. CTNI-85. GBM agile platform trial for newly diagnosed and recurrent GBM: results of first experimental arm, regorafenib. Neuro-Oncology. 2023;25(Supplement_5):v97-v8. This paper discussess the GBM Adaptive Global Innovative Learning Envrionment (GBM AGILE) trial, a novel trial designed to efficiency identify effective therapies in glioblastoma.
56.
Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396–401.PubMedCrossRef
57.
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756–60.PubMedCrossRef
58.
Rose M, Burgess JT, O’Byrne K, Richard DJ, Bolderson E. PARP inhibitors: clinical relevance, mechanisms of action and tumor resistance. Front Cell Dev Biol. 2020;8:564601.PubMedPubMedCentralCrossRef
59.
Sim HW, Galanis E, Khasraw M. PARP inhibitors in glioma: a review of therapeutic opportunities. Cancers (Basel). 2022;14(4):1003
60.
Ueno S, Sudo T, Hirasawa A. ATM: Functions of ATM kinase and its relevance to hereditary tumors. Int J Mol Sci. 2022;23(1):523
61.
Sim HW, McDonald KL, Lwin Z, Barnes EH, Rosenthal M, Foote MC, et al. A randomized phase II trial of veliparib, radiotherapy, and temozolomide in patients with unmethylated MGMT glioblastoma: the VERTU study. Neuro Oncol. 2021;23(10):1736–49.PubMedPubMedCentralCrossRef
62.
Weber JS, D’Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015;16(4):375–84.PubMedCrossRef
63.
Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373(1):23–34.PubMedPubMedCentralCrossRef
64.
Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WE, Poddubskaya E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373(2):123–35.PubMedPubMedCentralCrossRef
65.
Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375(19):1823–33.PubMedCrossRef
66.
Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–13.PubMedPubMedCentralCrossRef
67.
•• Sener U, Ruff MW, Campian JL. Immunotherapy in glioblastoma: current approaches and future perspectives. Int J Mol Sci. 2022;23(13):7046. This paper published in 2022 provides a comprehensive review of immunotherapy approaches previously and currently undergoing study in the setting of glioblastoma, addressing significant clinical trials and emphasizing molecular informed approaches to therapy.
68.
69.
Caccese M, Indraccolo S, Zagonel V, Lombardi G. PD-1/PD-L1 immune-checkpoint inhibitors in glioblastoma: a concise review. Crit Rev Oncol Hematol. 2019;135:128–34.PubMedCrossRef
70.
Reardon DA, Brandes AA, Omuro A, Mulholland P, Lim M, Wick 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(7):1003–10.PubMedCrossRef
71.
Omuro A, Brandes AA, Carpentier AF, Idbaih A, Reardon DA, Cloughesy T, et al. Radiotherapy combined with nivolumab or temozolomide for newly diagnosed glioblastoma with unmethylated MGMT promoter: an international randomized phase III trial. Neuro Oncol. 2023;25(1):123–34.PubMedCrossRef
72.
Lim M, Weller M, Idbaih A, Steinbach J, Finocchiaro G, Raval RR, et al. Phase III trial of chemoradiotherapy with temozolomide plus nivolumab or placebo for newly diagnosed glioblastoma with methylated MGMT promoter. Neuro Oncol. 2022;24(11):1935–49.PubMedPubMedCentralCrossRef
73.
Woroniecka K, Chongsathidkiet P, Rhodin K, Kemeny H, Dechant C, Farber SH, et al. T-cell exhaustion signatures vary with tumor type and are severe in glioblastoma. Clin Cancer Res. 2018;24(17):4175–86.PubMedPubMedCentralCrossRef
74.
• Chuntova P, Chow F, Watchmaker PB, Galvez M, Heimberger AB, Newell EW, et al. Unique challenges for glioblastoma immunotherapy-discussions across neuro-oncology and non-neuro-oncology experts in cancer immunology Meeting Report from the 2019 SNO Immuno-Oncology Think Tank. Neuro Oncol. 2021;23(3):356–75 (This report, derived from an expert meeting at the 2019 SNO Immuno-Oncology Think Tank, reviews special considerations of the utility of immunotherapy in glioblastoma, incorporting topics such as tumor microenvrionment, myeloid cells, T-cell dysfunction, cellular engineering and translation aspects of challenges unique to patients with primary brain tumors.).
75.
Grujic SD, O’Sullivan DD, Wehrmacher WH. Organizational control of hospital infrastructure determines the quality of care. Qual Assur Util Rev. 1989;4(1):19–24.PubMed
76.
Nduom EK, Wei J, Yaghi NK, Huang N, Kong LY, Gabrusiewicz K, et al. PD-L1 expression and prognostic impact in glioblastoma. Neuro Oncol. 2016;18(2):195–205.PubMedCrossRef
77.
Jackson CM, Choi J, Lim M. Mechanisms of immunotherapy resistance: lessons from glioblastoma. Nat Immunol. 2019;20(9):1100–9.PubMedCrossRef
78.
Platten M, Nollen EAA, Röhrig UF, Fallarino F, Opitz CA. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nat Rev Drug Discov. 2019;18(5):379–401.PubMedCrossRef
79.
80.
Chongsathidkiet P, Jackson C, Koyama S, Loebel F, Cui X, Farber SH, et al. Sequestration of T cells in bone marrow in the setting of glioblastoma and other intracranial tumors. Nat Med. 2018;24(9):1459–68.PubMedPubMedCentralCrossRef
81.
Nayak L, Molinaro AM, Peters K, Clarke JL, Jordan JT, de Groot J, et al. Randomized phase II and biomarker study of pembrolizumab plus bevacizumab versus pembrolizumab alone for patients with recurrent glioblastoma. Clin Cancer Res. 2021;27(4):1048–57.PubMedCrossRef
82.
Cloughesy TF, Mochizuki AY, Orpilla JR, Hugo W, Lee AH, Davidson TB, et al. Neoadjuvant anti-PD-1 immunotherapy promotes a survival benefit with intratumoral and systemic immune responses in recurrent glioblastoma. Nat Med. 2019;25(3):477–86.PubMedPubMedCentralCrossRef
83.
Schalper KA, Rodriguez-Ruiz ME, Diez-Valle R, López-Janeiro A, Porciuncula A, Idoate MA, et al. Neoadjuvant nivolumab modifies the tumor immune microenvironment in resectable glioblastoma. Nat Med. 2019;25(3):470–6.PubMedCrossRef
84.
Schumacher TN, Kesmir C, van Buuren MM. Biomarkers in cancer immunotherapy. Cancer Cell. 2015;27(1):12–4.PubMedCrossRef
85.
Chan TA, Wolchok JD, Snyder A. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med. 2015;373(20):1984.PubMedCrossRef
86.
Bouffet E, Larouche V, Campbell BB, Merico D, de Borja R, Aronson M, et al. Immune checkpoint inhibition for hypermutant glioblastoma multiforme resulting from germline biallelic mismatch repair deficiency. J Clin Oncol. 2016;34(19):2206–11.PubMedCrossRef
87.
Touat M, Li YY, Boynton AN, Spurr LF, Iorgulescu JB, Bohrson CL, et al. Mechanisms and therapeutic implications of hypermutation in gliomas. Nature. 2020;580(7804):517–23.PubMedPubMedCentralCrossRef
88.
Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med. 2016;375(9):819–29.PubMedPubMedCentralCrossRef
89.
Wilcox JA, Ramakrishna R, Magge R. Immunotherapy in glioblastoma. World Neurosurg. 2018;116:518–28.PubMedCrossRef
90.
De Jager R, Guinan P, Lamm D, Khanna O, Brosman S, De Kernion J, et al. Long-term complete remission in bladder carcinoma in situ with intravesical TICE bacillus Calmette Guerin. Overview analysis of six phase II clinical trials. Urology. 1991;38(6):507–13.PubMedCrossRef
91.
Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411–22.PubMedCrossRef
92.
Chesney JA, Ribas A, Long GV, Kirkwood JM, Dummer R, Puzanov I, et al. Randomized, double-blind, placebo-controlled, global phase III trial of talimogene laherparepvec combined with pembrolizumab for advanced melanoma. J Clin Oncol. 2023;41(3):528–40.PubMedCrossRef
93.
•• Neth BJ, Webb MJ, Parney IF, Sener UT. The current status, challenges, and future potential of therapeutic vaccination in glioblastoma. Pharmaceutics. 2023;15(4):1134. This paper published in 2023 provides a comprehensive review of the current status, challenges and future directions of vaccine therapies in glioblastoma.
94.
Saxena M, van der Burg SH, Melief CJM, Bhardwaj N. Therapeutic cancer vaccines. Nat Rev Cancer. 2021;21(6):360–78.PubMedCrossRef
95.
Binder DC, Ladomersky E, Lenzen A, Zhai L, Lauing KL, Otto-Meyer SD, et al. Lessons learned from rindopepimut treatment in patients with EGFRvIII-expressing glioblastoma. Transl Cancer Res. 2018;7(Suppl 4):S510–3.PubMedCrossRef
96.
Fenstermaker RA, Ciesielski MJ, Qiu J, Yang N, Frank CL, Lee KP, et al. Clinical study of a survivin long peptide vaccine (SurVaxM) in patients with recurrent malignant glioma. Cancer Immunol Immunother. 2016;65(11):1339–52.PubMedPubMedCentralCrossRef
97.
Spira A, Hansen AR, Harb WA, Curtis KK, Koga-Yamakawa E, Origuchi M, et al. Multicenter, open-label, phase I study of DSP-7888 dosing emulsion in patients with advanced malignancies. Target Oncol. 2021;16(4):461–9.PubMedPubMedCentralCrossRef
98.
Migliorini D, Dutoit V, Allard M, Grandjean Hallez N, Marinari E, Widmer V, et al. Phase I/II trial testing safety and immunogenicity of the multipeptide IMA950/poly-ICLC vaccine in newly diagnosed adult malignant astrocytoma patients. Neuro Oncol. 2019;21(7):923–33.PubMedPubMedCentralCrossRef
99.
100.
101.
Liau LM, Ashkan K, Tran DD, Campian JL, Trusheim JE, Cobbs CS, et al. First results on survival from a large phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma. J Transl Med. 2018;16(1):142.PubMedPubMedCentralCrossRef
102.
Preusser M, van den Bent MJ. Autologous tumor lysate-loaded dendritic cell vaccination (DCVax-L) in glioblastoma: breakthrough or fata morgana? Neuro Oncol. 2023;25(4):631–4.PubMedCrossRef
103.
Liau LM, Ashkan K, Brem S, Campian JL, Trusheim JE, Iwamoto FM, et al. Association of autologous tumor lysate-loaded dendritic cell vaccination with extension of survival among patients with newly diagnosed and recurrent glioblastoma: a phase 3 prospective externally controlled cohort trial. JAMA Oncol. 2023;9(1):112–21.PubMedCrossRef
104.
Wen PY, Reardon DA, Armstrong TS, Phuphanich S, Aiken RD, Landolfi JC, et al. A randomized double-blind placebo-controlled phase II trial of dendritic cell vaccine ICT-107 in newly diagnosed patients with glioblastoma. Clin Cancer Res. 2019;25(19):5799–807.PubMedPubMedCentralCrossRef
105.
Buchroithner J, Erhart F, Pichler J, Widhalm G, Preusser M, Stockhammer G, et al. Audencel immunotherapy based on dendritic cells has no effect on overall and progression-free survival in newly diagnosed glioblastoma: a phase II randomized trial. Cancers (Basel). 2018;10(10):372
106.
Cho DY, Yang WK, Lee HC, Hsu DM, Lin HL, Lin SZ, et al. Adjuvant immunotherapy with whole-cell lysate dendritic cells vaccine for glioblastoma multiforme: a phase II clinical trial. World Neurosurg. 2012;77(5–6):736–44.PubMedCrossRef
107.
Hilf N, Kuttruff-Coqui S, Frenzel K, Bukur V, Stevanović S, Gouttefangeas C, et al. Actively personalized vaccination trial for newly diagnosed glioblastoma. Nature. 2019;565(7738):240–5.PubMedCrossRef
108.
Keskin DB, Anandappa AJ, Sun J, Tirosh I, Mathewson ND, Li S, et al. Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Nature. 2019;565(7738):234–9.PubMedCrossRef
109.
Hodges TR, Ott M, Xiu J, Gatalica Z, Swensen J, Zhou S, et al. Mutational burden, immune checkpoint expression, and mismatch repair in glioma: implications for immune checkpoint immunotherapy. Neuro Oncol. 2017;19(8):1047–57.PubMedPubMedCentralCrossRef
110.
Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM. Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science. 1991;252(5007):854–6.PubMedCrossRef
111.
•• Webb MJ, Sener U, Vile RG. Current status and challenges of oncolytic virotherapy for the treatment of glioblastoma. Pharmaceuticals (Basel). 2023;16(6):793. This paper published in 2023 provides a comprehensive review of the current status and challenges of oncolytic viral therapy as therapy for glioblastoma.
112.
Stephenson KB, Barra NG, Davies E, Ashkar AA, Lichty BD. Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of anti-tumor immunity. Cancer Gene Ther. 2012;19(4):238–46.PubMedCrossRef
113.
Patel DM, Foreman PM, Nabors LB, Riley KO, Gillespie GY, Markert JM. Design of a phase I clinical trial to evaluate M032, a genetically engineered HSV-1 expressing IL-12, in patients with recurrent/progressive glioblastoma multiforme, anaplastic astrocytoma, or gliosarcoma. Hum Gene Ther Clin Dev. 2016;27(2):69–78.PubMedPubMedCentralCrossRef
114.
Wohlfahrt ME, Beard BC, Lieber A, Kiem HP. A capsid-modified, conditionally replicating oncolytic adenovirus vector expressing TRAIL Leads to enhanced cancer cell killing in human glioblastoma models. Cancer Res. 2007;67(18):8783–90.PubMedCrossRef
115.
Barrett JA, Cai H, Miao J, Khare PD, Gonzalez P, Dalsing-Hernandez J, et al. Regulated intratumoral expression of IL-12 using a RheoSwitch Therapeutic System(®) (RTS(®)) gene switch as gene therapy for the treatment of glioma. Cancer Gene Ther. 2018;25(5–6):106–16.PubMedPubMedCentralCrossRef
116.
Fyfe JA, Keller PM, Furman PA, Miller RL, Elion GB. Thymidine kinase from herpes simplex virus phosphorylates the new antiviral compound, 9-(2-hydroxyethoxymethyl)guanine. J Biol Chem. 1978;253(24):8721–7.PubMedCrossRef
117.
Eastham JA, Chen SH, Sehgal I, Yang G, Timme TL, Hall SJ, et al. Prostate cancer gene therapy: herpes simplex virus thymidine kinase gene transduction followed by ganciclovir in mouse and human prostate cancer models. Hum Gene Ther. 1996;7(4):515–23.PubMedCrossRef
118.
Wheeler LA, Manzanera AG, Bell SD, Cavaliere R, McGregor JM, Grecula JC, et al. Phase II multicenter study of gene-mediated cytotoxic immunotherapy as adjuvant to surgical resection for newly diagnosed malignant glioma. Neuro Oncol. 2016;18(8):1137–45.PubMedPubMedCentralCrossRef
119.
Ji N, Weng D, Liu C, Gu Z, Chen S, Guo Y, et al. Adenovirus-mediated delivery of herpes simplex virus thymidine kinase administration improves outcome of recurrent high-grade glioma. Oncotarget. 2016;7(4):4369–78.PubMedCrossRef
120.
Chiocca EA, Gelb AB, Chen CC, Rao G, Reardon DA, Wen PY, et al. Combined immunotherapy with controlled interleukin-12 gene therapy and immune checkpoint blockade in recurrent glioblastoma: an open-label, multi-institutional phase I trial. Neuro Oncol. 2022;24(6):951–63.PubMedCrossRef
121.
Lang FF, Conrad C, Gomez-Manzano C, Yung WKA, Sawaya R, Weinberg JS, et al. Phase I study of DNX-2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J Clin Oncol. 2018;36(14):1419–27.PubMedPubMedCentralCrossRef
122.
Todo T, Ino Y, Ohtsu H, Shibahara J, Tanaka M. A phase I/II study of triple-mutated oncolytic herpes virus G47∆ in patients with progressive glioblastoma. Nat Commun. 2022;13(1):4119.PubMedPubMedCentralCrossRef
123.
Todo T, Ito H, Ino Y, Ohtsu H, Ota Y, Shibahara J, et al. Intratumoral oncolytic herpes virus G47∆ for residual or recurrent glioblastoma: a phase 2 trial. Nat Med. 2022;28(8):1630–9.PubMedPubMedCentralCrossRef
124.
Gromeier M, Lachmann S, Rosenfeld MR, Gutin PH, Wimmer E. Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci U S A. 2000;97(12):6803–8.PubMedPubMedCentralCrossRef
125.
Desjardins A, Gromeier M, Herndon JE 2nd, Beaubier N, Bolognesi DP, Friedman AH, et al. Recurrent glioblastoma treated with recombinant poliovirus. N Engl J Med. 2018;379(2):150–61.PubMedPubMedCentralCrossRef
126.
Cloughesy TF, Petrecca K, Walbert T, Butowski N, Salacz M, Perry J, et al. Effect of vocimagene amiretrorepvec in combination with flucytosine vs standard of care on survival following tumor resection in patients with recurrent high-grade glioma: a randomized clinical trial. JAMA Oncol. 2020;6(12):1939–46.PubMedCrossRef
127.
Mihelson N, McGavern DB. Viral control of glioblastoma. Viruses. 2021;13(7):1264
128.
Zhu Z, Gorman MJ, McKenzie LD, Chai JN, Hubert CG, Prager BC, et al. Zika virus has oncolytic activity against glioblastoma stem cells. J Exp Med. 2017;214(10):2843–57.PubMedPubMedCentralCrossRef
129.
Zhu Z, Mesci P, Bernatchez JA, Gimple RC, Wang X, Schafer ST, et al. Zika virus targets glioblastoma stem cells through a SOX2-integrin α(v)β(5) axis. Cell Stem Cell. 2020;26(2):187-204.e10.PubMedPubMedCentralCrossRef
130.
Nair S, Mazzoccoli L, Jash A, Govero J, Bais SS, Hu T, et al. Zika virus oncolytic activity requires CD8+ T cells and is boosted by immune checkpoint blockade. JCI Insight. 2021;6(1):e144619
131.
Collins SA, Shah AH, Ostertag D, Kasahara N, Jolly DJ. Clinical development of retroviral replicating vector Toca 511 for gene therapy of cancer. Expert Opin Biol Ther. 2021;21(9):1199–214.PubMedPubMedCentralCrossRef
132.
Friedmann-Morvinski D. Glioblastoma heterogeneity and cancer cell plasticity. Crit Rev Oncog. 2014;19(5):327–36.PubMedCrossRef
133.
Evgin L, Vile RG. Parking CAR T cells in tumours: oncolytic viruses as valets or vandals? Cancers (Basel). 2021;13(5):1106
134.
135.
136.
137.
Bagley SJ, Desai AS, Linette GP, June CH, O’Rourke DM. CAR T-cell therapy for glioblastoma: recent clinical advances and future challenges. Neuro Oncol. 2018;20(11):1429–38.PubMedPubMedCentralCrossRef
138.
Raje N, Berdeja J, Lin Y, Siegel D, Jagannath S, Madduri D, et al. Anti-BCMA CAR T-cell therapy bb2121 in relapsed or refractory multiple myeloma. N Engl J Med. 2019;380(18):1726–37.PubMedPubMedCentralCrossRef
139.
Maggs L, Cattaneo G, Dal AE, Moghaddam AS, Ferrone S. CAR T cell-based immunotherapy for the treatment of glioblastoma. Front Neurosci. 2021;15:662064.PubMedPubMedCentralCrossRef
140.
Goff SL, Morgan RA, Yang JC, Sherry RM, Robbins PF, Restifo NP, et al. Pilot trial of adoptive transfer of chimeric antigen receptor-transduced T cells targeting EGFRvIII in patients with glioblastoma. J Immunother. 2019;42(4):126–35.PubMedPubMedCentralCrossRef
141.
O'Rourke DM, Nasrallah MP, Desai A, Melenhorst JJ, Mansfield K, Morrissette JJD, et al. A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma. Sci Transl Med 2017;9(399):eaaa0984
142.
Brown CE, Badie B, Barish ME, Weng L, Ostberg JR, Chang WC, et al. Bioactivity and safety of IL13Rα2-redirected chimeric antigen receptor CD8+ T cells in patients with recurrent glioblastoma. Clin Cancer Res. 2015;21(18):4062–72.PubMedPubMedCentralCrossRef
143.
Mineo JF, Bordron A, Baroncini M, Maurage CA, Ramirez C, Siminski RM, et al. Low HER2-expressing glioblastomas are more often secondary to anaplastic transformation of low-grade glioma. J Neurooncol. 2007;85(3):281–7.PubMedCrossRef
144.
Ahmed N, Brawley V, Hegde M, Bielamowicz K, Kalra M, Landi D, et al. HER2-specific chimeric antigen receptor-modified virus-specific T cells for progressive glioblastoma: a phase 1 dose-escalation trial. JAMA Oncol. 2017;3(8):1094–101.PubMedPubMedCentralCrossRef
145.
Press MF, Cordon-Cardo C, Slamon DJ. Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene. 1990;5(7):953–62.PubMed
146.
Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther. 2010;18(4):843–51.PubMedPubMedCentralCrossRef
147.
148.
Kontos F, Michelakos T, Kurokawa T, Sadagopan A, Schwab JH, Ferrone CR, et al. B7–H3: an attractive target for antibody-based immunotherapy. Clin Cancer Res. 2021;27(5):1227–35.PubMedCrossRef
149.
Picarda E, Ohaegbulam KC, Zang X. Molecular pathways: targeting B7–H3 (CD276) for human cancer immunotherapy. Clin Cancer Res. 2016;22(14):3425–31.PubMedPubMedCentralCrossRef
150.
Seaman S, Zhu Z, Saha S, Zhang XM, Yang MY, Hilton MB, et al. Eradication of tumors through simultaneous ablation of CD276/B7-H3-positive tumor cells and tumor vasculature. Cancer Cell. 2017;31(4):501-15.e8.PubMedPubMedCentralCrossRef
151.
Tang X, Zhao S, Zhang Y, Wang Y, Zhang Z, Yang M, et al. B7–H3 as a Novel CAR-T therapeutic target for glioblastoma. Mol Ther Oncolytics. 2019;14:279–87.PubMedPubMedCentralCrossRef
152.
Xiong L, Edwards CK 3rd, Zhou L. The biological function and clinical utilization of CD147 in human diseases: a review of the current scientific literature. Int J Mol Sci. 2014;15(10):17411–41.PubMedPubMedCentralCrossRef
153.
154.
Golinelli G, Grisendi G, Prapa M, Bestagno M, Spano C, Rossignoli F, et al. Targeting GD2-positive glioblastoma by chimeric antigen receptor empowered mesenchymal progenitors. Cancer Gene Ther. 2020;27(7–8):558–70.PubMedCrossRef
155.
Prapa M, Caldrer S, Spano C, Bestagno M, Golinelli G, Grisendi G, et al. A novel anti-GD2/4-1BB chimeric antigen receptor triggers neuroblastoma cell killing. Oncotarget. 2015;6(28):24884–94.PubMedPubMedCentralCrossRef
156.
Mount CW, Majzner RG, Sundaresh S, Arnold EP, Kadapakkam M, Haile S, et al. Potent antitumor efficacy of anti-GD2 CAR T cells in H3–K27M(+) diffuse midline gliomas. Nat Med. 2018;24(5):572–9.PubMedPubMedCentralCrossRef
157.
DeBin JA, Maggio JE, Strichartz GR. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am J Physiol. 1993;264(2 Pt 1):C361–9.PubMedCrossRef
158.
Lyons SA, O’Neal J, Sontheimer H. Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia. 2002;39(2):162–73.PubMedCrossRef
159.
Wang D, Starr R, Chang WC, Aguilar B, Alizadeh D, Wright SL, et al. Chlorotoxin-directed CAR T cells for specific and effective targeting of glioblastoma. Sci Transl Med. 2020;12(533):eaaw2672
160.
Grant SJ, Grimshaw AA, Silberstein J, Murdaugh D, Wildes TM, Rosko AE, et al. Clinical presentation, risk factors, and outcomes of immune effector cell-associated neurotoxicity syndrome following chimeric antigen receptor T cell therapy: a systematic review. Transplant Cell Ther. 2022;28(6):294–302.PubMedPubMedCentralCrossRef
161.
Garcia Borrega J, Gödel P, Rüger MA, Onur ÖA, Shimabukuro-Vornhagen A, Kochanek M, et al. In the eye of the storm: immune-mediated toxicities associated with CAR-T cell therapy. Hemasphere. 2019;3(2):e191.PubMedPubMedCentralCrossRef
162.
Mackall CL, Miklos DB. CNS endothelial cell activation emerges as a driver of CAR T cell-associated neurotoxicity. Cancer Discov. 2017;7(12):1371–3.PubMedCrossRef
163.
164.
Brown CE, Alizadeh D, Starr R, Weng L, Wagner JR, Naranjo A, et al. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med. 2016;375(26):2561–9.PubMedPubMedCentralCrossRef
165.
Vanderlugt CL, Miller SD. Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat Rev Immunol. 2002;2(2):85–95.PubMedCrossRef
166.
Jin L, Tao H, Karachi A, Long Y, Hou AY, Na M, et al. CXCR1- or CXCR2-modified CAR T cells co-opt IL-8 for maximal antitumor efficacy in solid tumors. Nat Commun. 2019;10(1):4016.PubMedPubMedCentralCrossRef
167.
Juillerat A, Marechal A, Filhol JM, Valogne Y, Valton J, Duclert A, et al. An oxygen sensitive self-decision making engineered CAR T-cell. Sci Rep. 2017;7:39833.PubMedPubMedCentralCrossRef
168.
Zhang C, Burger MC, Jennewein L, Genßler S, Schönfeld K, Zeiner P, et al. ErbB2/HER2-specific NK cells for targeted therapy of glioblastoma. J Natl Cancer Inst. 2016;108(5)
169.
Alkins R, Burgess A, Ganguly M, Francia G, Kerbel R, Wels WS, et al. Focused ultrasound delivers targeted immune cells to metastatic brain tumors. Cancer Res. 2013;73(6):1892–9.PubMedPubMedCentralCrossRef
170.
Hersh AM, Bhimreddy M, Weber-Levine C, Jiang K, Alomari S, Theodore N, et al. Applications of focused ultrasound for the treatment of glioblastoma: a new frontier. Cancers (Basel). 2022;14(19):4920
171.
Elhelf IAS, Albahar H, Shah U, Oto A, Cressman E, Almekkawy M. High intensity focused ultrasound: the fundamentals, clinical applications and research trends. Diagn Interv Imaging. 2018;99(6):349–59.PubMedCrossRef
172.
Fomenko A, Lozano AM. Neuromodulation and ablation with focused ultrasound - toward the future of noninvasive brain therapy. Neural Regen Res. 2019;14(9):1509–10.PubMedPubMedCentralCrossRef
173.
• Roberts JW, Powlovich L, Sheybani N, LeBlang S. Focused ultrasound for the treatment of glioblastoma. J Neurooncol. 2022;157(2):237–47 (This paper, published in 2022, reviews outcomes of the 2021 workshop sponsored by the Focused Ultrasound Foundation to discuss the landscape of focused ultrasound therapy as a new therapy for treating glioblastoma).
174.
Park SH, Kim MJ, Jung HH, Chang WS, Choi HS, Rachmilevitch I, et al. One-year outcome of multiple blood-brain barrier disruptions with temozolomide for the treatment of glioblastoma. Front Oncol. 2020;10:1663.PubMedPubMedCentralCrossRef
175.
Mainprize T, Lipsman N, Huang Y, Meng Y, Bethune A, Ironside S, et al. Blood-brain barrier opening in primary brain tumors with non-invasive MR-guided focused ultrasound: a clinical safety and feasibility study. Sci Rep. 2019;9(1):321.PubMedPubMedCentralCrossRef
176.
D’Ammando A, Raspagliesi L, Gionso M, Franzini A, Porto E, Di Meco F, et al. Sonodynamic therapy for the treatment of intracranial gliomas. J Clin Med. 2021;10(5):1101
177.
Schneider CS, Woodworth GF, Vujaskovic Z, Mishra MV. Radiosensitization of high-grade gliomas through induced hyperthermia: review of clinical experience and the potential role of MR-guided focused ultrasound. Radiother Oncol. 2020;142:43–51.PubMedCrossRef
178.
Lu G, Wang X, Li F, Wang S, Zhao J, Wang J, et al. Engineered biomimetic nanoparticles achieve targeted delivery and efficient metabolism-based synergistic therapy against glioblastoma. Nat Commun. 2022;13(1):4214.PubMedPubMedCentralCrossRef
179.
180.
Cai Q, Li X, Xiong H, Fan H, Gao X, Vemireddy V, et al. Optical blood-brain-tumor barrier modulation expands therapeutic options for glioblastoma treatment. Nat Commun. 2023;14(1):4934.PubMedPubMedCentralCrossRef
181.
Malouff TD, Peterson JL, Mahajan A, Trifiletti DM. Carbon ion radiotherapy in the treatment of gliomas: a review. J Neurooncol. 2019;145(2):191–9.PubMedCrossRef
182.
Suzuki M, Kase Y, Kanai T, Ando K. Correlation between cell death and induction of non-rejoining PCC breaks by carbon-ion beams. Adv Space Res. 1998;22(4):561–8.PubMedCrossRef
183.
Chiblak S, Campos B, Gal Z, Tang Z, Brons S, Unterberg A, et al. Photon versus proton versus carbon irradiation of glioma initiating cells. International Journal of Radiation Oncol*Biol*Phys. 2012;84(3, Supplement):S677
184.
Rackwitz T, Debus J. Clinical applications of proton and carbon ion therapy. Semin Oncol. 2019;46(3):226–32.PubMedCrossRef
185.
Combs SE, Kieser M, Rieken S, Habermehl D, Jäkel O, Haberer T, et al. Randomized phase II study evaluating a carbon ion boost applied after combined radiochemotherapy with temozolomide versus a proton boost after radiochemotherapy with temozolomide in patients with primary glioblastoma: the CLEOPATRA trial. BMC Cancer. 2010;10:478.PubMedPubMedCentralCrossRef
186.
van Solinge TS, Nieland L, Chiocca EA, Broekman MLD. Advances in local therapy for glioblastoma - taking the fight to the tumour. Nat Rev Neurol. 2022;18(4):221–36.PubMedPubMedCentralCrossRef
187.
Cifarelli CP, Jacobson GM. Intraoperative radiotherapy in brain malignancies: indications and outcomes in primary and metastatic brain tumors. Front Oncol. 2021;11:768168.PubMedPubMedCentralCrossRef
188.
Usychkin S, Calvo F, dos Santos MA, Samblás J, de Urbina DO, Bustos JC, et al. Intra-operative electron beam radiotherapy for newly diagnosed and recurrent malignant gliomas: feasibility and long-term outcomes. Clin Transl Oncol. 2013;15(1):33–8.PubMedCrossRef
189.
Waters JD, Rose B, Gonda DD, Scanderbeg DJ, Russell M, Alksne JF, et al. Immediate post-operative brachytherapy prior to irradiation and temozolomide for newly diagnosed glioblastoma. J Neurooncol. 2013;113:467–77.PubMedCrossRef
190.
Budnick HC, Richardson AM, Shiue K, Watson G, Ng SK, Le Y, et al. GammaTile for gliomas: a single-center case series. Cureus. 2021;13(11):e19390.PubMedPubMedCentral
191.
Brachman DG, Youssef E, Dardis CJ, Sanai N, Zabramski JM, Smith KA, et al. Resection and permanent intracranial brachytherapy using modular, biocompatible cesium-131 implants: results in 20 recurrent, previously irradiated meningiomas. J Neurosurg. 2018;131(6):1819–28.PubMedCrossRef
192.
Brachman D, Youssef E, Dardis C, Smith K, Pinnaduwage D, Nakaji P. Surgically targeted radiation therapy: safety profile of collagen tile brachytherapy in 79 recurrent, previously irradiated intracranial neoplasms on a prospective clinical trial. Brachytherapy. 2019;18(3):S35–6.CrossRef
193.
Ferreira C, Sterling D, Reynolds M, Dusenbery K, Chen C, Alaei P. First clinical implementation of GammaTile permanent brain implants after FDA clearance. Brachytherapy. 2021;20(3):673–85.PubMedCrossRef
194.
Greenwald J, Taube S, Yondorf MZ, Smith A, Sabbas A, Wernicke AG. Placement of (131)Cs permanent brachytherapy seeds in a large combined cavity of two resected brain metastases in one setting: case report and technical note. J Contemp Brachytherapy. 2019;11(4):356–60.PubMedPubMedCentralCrossRef
195.
Gessler DJ, Ferreira C, Dusenbery K, Chen CC. GammaTile(®): surgically targeted radiation therapy for glioblastomas. Future Oncol. 2020;16(30):2445–55.PubMedCrossRef
196.
197.
198.
Lidar Z, Mardor Y, Jonas T, Pfeffer R, Faibel M, Nass D, et al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J Neurosurg. 2004;100(3):472–9.PubMedCrossRef
199.
Bruce JN, Fine RL, Canoll P, Yun J, Kennedy BC, Rosenfeld SS, et al. Regression of recurrent malignant gliomas with convection-enhanced delivery of topotecan. Neurosurgery. 2011;69(6):1272–9; discussion 9–80
200.
Jahangiri A, Chin AT, Flanigan PM, Chen R, Bankiewicz K, Aghi MK. Convection-enhanced delivery in glioblastoma: a review of preclinical and clinical studies. J Neurosurg. 2017;126(1):191–200.PubMedCrossRef
201.
Kunwar S, Chang S, Westphal M, Vogelbaum M, Sampson J, Barnett G, et al. Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol. 2010;12(8):871–81.PubMedPubMedCentralCrossRef
202.
Dewey RA, Morrissey G, Cowsill CM, Stone D, Bolognani F, Dodd NJ, et al. Chronic brain inflammation and persistent herpes simplex virus 1 thymidine kinase expression in survivors of syngeneic glioma treated by adenovirus-mediated gene therapy: implications for clinical trials. Nat Med. 1999;5(11):1256–63.PubMedCrossRef
203.
Brown MC, Holl EK, Boczkowski D, Dobrikova E, Mosaheb M, Chandramohan V, et al. Cancer immunotherapy with recombinant poliovirus induces IFN-dominant activation of dendritic cells and tumor antigen-specific CTLs. Sci Transl Med 2017;9(408):eaan4220
204.
Fabian D, Guillermo Prieto Eibl MDP, Alnahhas I, Sebastian N, Giglio P, Puduvalli V, et al. Treatment of glioblastoma (GBM) with the addition of tumor-treating fields (TTF): a review. Cancers (Basel). 2019;11(2):174
205.
Vanderbeek AM, Rahman R, Fell G, Ventz S, Chen T, Redd R, et al. The clinical trials landscape for glioblastoma: is it adequate to develop new treatments? Neuro Oncol. 2018;20(8):1034–43.PubMedPubMedCentralCrossRef
206.
Lee EQ, Chukwueke UN, Hervey-Jumper SL, de Groot JF, Leone JP, Armstrong TS, et al. Barriers to accrual and enrollment in brain tumor trials. Neuro Oncol. 2019;21(9):1100–17.PubMedPubMedCentral
207.
Bates AJ, Couillard SA, Arons DF, Yung WKA, Vogelbaum M, Wen PY, et al. HOUT-15. Brain tumor patient and caregiver survey on clinical trials: identifying attitudes and barriers to patient participation. Neuro Oncol. 2017;19(Suppl 6):vi109
208.
Rahman R, Trippa L, Lee EQ, Arrillaga-Romany I, Fell G, Touat M, et al. Inaugural results of the individualized screening trial of innovative glioblastoma therapy: a phase II platform trial for newly diagnosed glioblastoma using Bayesian adaptive randomization. J Clin Oncol. 2023;41(36):5524–35.PubMedCrossRef
209.
Ban H, Obonai T, Mishima Y, Matsumoto N, Mie M, Nakamura N. A novel humanized antibody targeting CD39 that enhances anti-tumor immunity and the efficacy of cancer immunotherapy. J Clin Oncol. 2022;40(16_suppl):e14508-e
210.
Wick W, Dettmer S, Berberich A, Kessler T, Karapanagiotou-Schenkel I, Wick A, et al. N2M2 (NOA-20) phase I/II trial of molecularly matched targeted therapies plus radiotherapy in patients with newly diagnosed non-MGMT hypermethylated glioblastoma. Neuro Oncol. 2019;21(1):95–105.PubMedCrossRef
211.
Kong BY, Sim HW, Barnes EH, Nowak AK, Hovey EJ, Jeffree R, et al. Multi-Arm GlioblastoMa Australasia (MAGMA): protocol for a multiarm randomised clinical trial for people affected by glioblastoma. BMJ Open. 2022;12(9):e058107.PubMedPubMedCentralCrossRef
212.
Dorsey ER, Kluger B, Lipset CH. The new normal in clinical trials: decentralized studies. Ann Neurol. 2020;88(5):863–6.PubMedCrossRef
Metadata
Title
Novel Clinical Trials and Approaches in the Management of Glioblastoma
Authors
Allison R. Valerius
Lauren M. Webb
Ugur Sener
Publication date
28-03-2024
Publisher
Springer US
Published in
Current Oncology Reports / Issue 5/2024
Print ISSN: 1523-3790
Electronic ISSN: 1534-6269
DOI
https://doi.org/10.1007/s11912-024-01519-4

Other articles of this Issue 5/2024

Current Oncology Reports 5/2024 Go to the issue

ReviewPaper

Ovarian Suppression: Early Menopause, Late Effects

REVIEW

Perioperative Neurocognitive Function in Glioma Surgery

REVIEW

Radionuclide Theranostics in Neuroendocrine Neoplasms: An Update

REVIEW

Patient Navigation in Cancer Treatment: A Systematic Review

REVIEW

Advances in radionuclide therapies for neuroendocrine tumors

REVIEW

Current Trends and Challenges of Microbiome Research in Prostate Cancer
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits