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Neoadjuvant immune checkpoint inhibition in the management of glioblastoma: Exploring a new frontier

Frederico, Stephen C., Darling, Corbin, Bielanin, John P., Dubinsky, Alexandra C., Zhang, Xiaoran, Hadjipanayis, Constantinos G., Kohanbash, Gary·2023·Frontiers in Immunology
DOI 10.3389/fimmu.2023.1057567PMC PMC9981631
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Abstract

Brain tumors are one of the leading causes of cancer related death in both the adult and pediatric patient population. Gliomas represent a cohort of brain tumors derived from glial cell lineages which include astrocytomas, oligodendrogliomas and glioblastomas (GBMs). These tumors are known to grow aggressively and have a high lethality with GBM being the most aggressive tumor in this group. Currently, few treatment options exist for GBM outside of surgical resection, radiation therapy and chemotherapy. While these measures have been shown to marginally improve patient survival, patients, especially those diagnosed with GBM, often experience a recurrence of their disease. Following disease recurrence, treatment options become more limited as additional surgical resections can pose life threatening risk to the patient, patients may be ineligible for additional radiation, and the recurrent tumor may be resistant to chemotherapy. Immune checkpoint inhibitors (ICIs) have revolutionized the field of cancer immunotherapy as many patients with cancers residing outside the central nervous system (CNS) have experienced a survival benefit from this treatment modality. It has often been observed that this survival benefit is increased following neoadjuvant administration of immune checkpoint inhibitors as tumor antigen is still present in the patient which enables a more robust anti-tumor immune response. Interestingly, results for ICI-based studies for patients with GBM have been largely disappointing which is a stark contrast from the success this treatment modality has had in non-central nervous system cancers. In this review, we will discuss the various benefits of neoadjuvant immune checkpoint inhibition such as how this approach reduces tumor burden and allows for a greater induction of an anti-tumor immune response. Additionally, we will discuss several non-CNS cancers where neoadjuvant immune checkpoint inhibition has been successful and discuss why we believe this approach may provide a survival benefit for GBM patients. We hope this manuscript will foster future studies aimed at exploring whether this approach may be beneficial for patients diagnosed with GBM.

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Research works printed but not linked: 73

  1. Ostrom, 2020, CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the united states in 2013-2017, Neuro-oncology., 22, iv1, 10.1093/neuonc/noaa200 · DOI
  2. Louis, 2006, Molecular pathology of malignant gliomas, Annu Rev Pathol, 1, 97, 10.1146/annurev.pathol.1.110304.100043 · DOI
  3. Louis, 2021, The 2021 WHO classification of tumors of the central nervous system: a summary, Neuro Oncol, 23, 10.1093/neuonc/noab106 · DOI · Paper page
  4. Kurokawa, 2022, Major changes in 2021 world health organization classification of central nervous system tumors, RadioGraphics., 42, 10.1148/rg.210236 · DOI
  5. Ohgaki, 2005, Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas, J Neuropathol Exp Neurol, 64, 10.1093/jnen/64.6.479 · DOI
  6. Van den Bent, 2008, Oligodendroglioma, Crit Rev Oncol Hematol, 66, 10.1016/j.critrevonc.2007.11.007 · DOI
  7. Buckner, 2003, Factors influencing survival in high-grade gliomas, Semin Oncol, 30, 10.1053/j.seminoncol.2003.11.031 · DOI
  8. Kim, 2019, The Korean society for neuro-oncology (KSNO) guideline for WHO grade II cerebral gliomas in adults: Version 2019.01, Brain Tumor Res Treat, 7, 74, 10.14791/btrt.2019.7.e43 · DOI
  9. Ostrom, 2019, CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the united states in 2012-2016, Neuro Oncol, 21, v1, 10.1093/neuonc/noz150 · DOI
  10. Frederico, 2021, Making a cold tumor hot: The role of vaccines in the treatment of glioblastoma, Front Oncol, 11, 10.3389/fonc.2021.672508 · DOI
  11. Claes, 2007, Diffuse glioma growth: a guerilla war, Acta Neuropathol., 114, 10.1007/s00401-007-0293-7 · DOI
  12. Ratnam, 2020, Clinical correlates for immune checkpoint therapy: significance for CNS malignancies, Neuro-Oncology Advances., 3, 10.1093/noajnl/vdaa161 · DOI
  13. Frederico, 2023, Pre-clinical models for evaluating glioma targeted immunotherapies, Front Immunol, 13, 10.3389/fimmu.2022.1092399 · DOI
  14. Harjunpää, 2019, Cell adhesion molecules and their roles and regulation in the immune and tumor microenvironment, Front Immunol, 10, 10.3389/fimmu.2019.01078 · DOI
  15. Monu, 2012, Myeloid-derived suppressor cells and anti-tumor T cells: a complex relationship, Immunol Invest, 41, 595, 10.3109/08820139.2012.673191 · DOI
  16. Pearson, 2020, Immune escape in glioblastoma multiforme and the adaptation of immunotherapies for treatment, Front Immunol, 11, 10.3389/fimmu.2020.582106 · DOI
  17. Woroniecka, 2018, T-Cell exhaustion in glioblastoma, Oncotarget., 9, 10.18632/oncotarget.26228 · DOI
  18. Giles, 2018, Dexamethasone-induced immunosuppression: mechanisms and implications for immunotherapy, J ImmunoTherapy Cancer., 6, 51, 10.1186/s40425-018-0371-5 · DOI
  19. Parker, 2015, Molecular heterogeneity in glioblastoma: Potential clinical implications, Front Oncol, 5, 10.3389/fonc.2015.00055 · DOI
  20. Soeda, 2015, The evidence of glioblastoma heterogeneity, Sci Rep, 5, 7979, 10.1038/srep07979 · DOI
  21. Dirkse, 2019, Stem cell-associated heterogeneity in glioblastoma results from intrinsic tumor plasticity shaped by the microenvironment, Nat Commun, 10, 1787, 10.1038/s41467-019-09853-z · DOI
  22. Behnan, 2019, The landscape of the mesenchymal signature in brain tumours, Brain., 142, 10.1093/brain/awz044 · DOI
  23. Akindona, 2022, Exploring the origin of the cancer stem cell niche and its role in anti-angiogenic treatment for glioblastoma, Front Oncol, 12, 10.3389/fonc.2022.947634 · DOI
  24. Kniesel, 2000, Tight junctions of the blood-brain barrier, Cell Mol Neurobiol, 20, 57, 10.1023/A:1006995910836 · DOI
  25. Wesolowski, 2010, Temozolomide (Temodar), AJNR Am J Neuroradiol, 31, 10.3174/ajnr.A2170 · DOI
  26. Reardon, 2020, Effect of nivolumab vs. bevacizumab in patients with recurrent glioblastoma: The CheckMate 143 phase 3 randomized clinical trial, JAMA Oncol, 6, 10.1001/jamaoncol.2020.1024 · DOI
  27. Ratnam, 2021, Reversing epigenetic gene silencing to overcome immune evasion in CNS malignancies, Front Oncol, 11, 10.3389/fonc.2021.719091 · DOI
  28. Lim, 2022, Phase III trial of chemoradiotherapy with temozolomide plus nivolumab or placebo for newly diagnosed glioblastoma with methylated MGMT promoter, Neuro Oncol, 24, 10.1093/neuonc/noac116 · DOI
  29. Weller, 2017, Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial, Lancet Oncol, 18, 10.1016/S1470-2045(17)30517-X · DOI
  30. Datsi, 2021, Dendritic cell vaccination of glioblastoma: Road to success or dead end, Front Immunol, 12, 10.3389/fimmu.2021.770390 · DOI
  31. Kong, 2018, Vaccination in the immunotherapy of glioblastoma, Hum Vaccin Immunother., 14, 10.1080/21645515.2017.1388481 · DOI
  32. Xu, 2014, Current vaccine trials in glioblastoma: A review, J Immunol Res, 2014, 796856, 10.1155/2014/796856 · DOI
  33. Cloughesy, 2019, Neoadjuvant anti-PD-1 immunotherapy promotes a survival benefit with intratumoral and systemic immune responses in recurrent glioblastoma, Nat Med, 25, 10.1038/s41591-018-0337-7 · DOI · Paper page
  34. Xu, 2021, Neoadjuvant immunotherapy facilitates resection of surgically-challenging lung squamous cell cancer, J Thorac Dis, 13, 10.21037/jtd-21-1195 · DOI
  35. Rosenberg, 2014, IL-2: the first effective immunotherapy for human cancer, J Immunol, 192, 10.4049/jimmunol.1490019 · DOI
  36. Gershenwald, 2018, Melanoma staging: American joint committee on cancer (AJCC) 8th edition and beyond, Ann Surg Oncol, 25, 10.1245/s10434-018-6513-7 · DOI
  37. Robert, 2015, Improved overall survival in melanoma with combined dabrafenib and trametinib, N Engl J Med, 372, 10.1056/NEJMoa1412690 · DOI
  38. Hodi, 2010, Improved survival with ipilimumab in patients with metastatic melanoma, N Engl J Med, 363, 10.1056/NEJMoa1003466 · DOI · Paper page
  39. Robert, 2015, Nivolumab in previously untreated melanoma without BRAF mutation, N Engl J Med, 372, 10.1056/NEJMoa1412082 · DOI · Paper page
  40. ClinicalTrials.gov Bethesda (MD)
  41. Song, 2020, Neoadjuvant versus adjuvant immune checkpoint blockade in the treatment of clinical stage III melanoma, Ann Surg Oncol, 27, 10.1245/s10434-019-08174-1 · DOI
  42. Amaria, 2018, Author correction: Neoadjuvant immune checkpoint blockade in high-risk resectable melanoma, Nat Med, 24, 1941, 10.1038/s41591-018-0251-z · DOI
  43. Blank, 2018, Neoadjuvant versus adjuvant ipilimumab plus nivolumab in macroscopic stage III melanoma, Nat Med, 24, 10.1038/s41591-018-0198-0 · DOI · Paper page
  44. Westphal, 2017, Molecular insights into melanoma brain metastases, Cancer., 123, 10.1002/cncr.30594 · DOI
  45. Goldberg, 2016, Pembrolizumab for patients with melanoma or non-small-cell lung cancer and untreated brain metastases: early analysis of a non-randomised, open-label, phase 2 trial, Lancet Oncol, 17, 10.1016/S1470-2045(16)30053-5 · DOI
  46. Tawbi, 2021, Long-term outcomes of patients with active melanoma brain metastases treated with combination nivolumab plus ipilimumab (CheckMate 204): final results of an open-label, multicentre, phase 2 study, Lancet Oncol, 22, 10.1016/S1470-2045(21)00545-3 · DOI
  47. Lee, 2021, PS01.05 surgical and clinical outcomes with neoadjuvant atezolizumab in resectable stage IB–IIIB NSCLC: LCMC3 trial primary analysis, J Thorac Oncol, 16, 10.1016/j.jtho.2021.01.320 · DOI
  48. Kwiatkowski, 2019, Neoadjuvant atezolizumab in resectable non-small cell lung cancer (NSCLC): Interim analysis and biomarker data from a multicenter study (LCMC3), J Clin Oncol, 37, 8503, 10.1200/JCO.2019.37.15_suppl.8503 · DOI · Paper page
  49. Roller, 2022, Exploring the evolving scope of neoadjuvant immunotherapy in NSCLC, Cancers (Basel)., 14, 10.3390/cancers14030741 · DOI
  50. Reuss, 2020, Neoadjuvant nivolumab plus ipilimumab in resectable non-small cell lung cancer, J ImmunoTherapy Cancer., 8, 10.1136/jitc-2020-001282 · DOI
  51. Eichhorn, 2019, Neoadjuvant anti-programmed death-1 immunotherapy by pembrolizumab in resectable nodal positive stage II/IIIa non-small-cell lung cancer (NSCLC): the NEOMUN trial, BMC Cancer., 19, 413, 10.1186/s12885-019-5624-2 · DOI
  52. Zhao, 2020, Breast cancer immunology and immunotherapy: targeting the programmed cell death protein-1/programmed cell death protein ligand-1, Chin Med J (Engl), 133, 10.1097/CM9.0000000000000710 · DOI
  53. DeMichele, 2015, The neoadjuvant model is still the future for drug development in breast cancer, Clin Cancer Res, 21, 10.1158/1078-0432.CCR-14-1760 · DOI
  54. Berruti, 2014, Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: a meta-regression of 29 randomized prospective studies, J Clin Oncol, 32, 10.1200/JCO.2014.55.2836 · DOI
  55. Sumransub, 2021, Advances and new frontiers for immunotherapy in colorectal cancer: Setting the stage for neoadjuvant success, Mol Ther Oncolytics, 22, 1, 10.1016/j.omto.2021.05.001 · DOI
  56. Abdul-Latif, 2020, Immunotherapy in gastrointestinal cancer: The current scenario and future perspectives, Cancer Treat Rev, 88, 102030, 10.1016/j.ctrv.2020.102030 · DOI
  57. Grothey, 2020, Pembrolizumab in MSI-H-dMMR advanced colorectal cancer - a new standard of care, N Engl J Med, 383, 10.1056/NEJMe2031294 · DOI
  58. Chalabi, 2020, Neoadjuvant immunotherapy leads to pathological responses in MMR-proficient and MMR-deficient early-stage colon cancers, Nat Med, 26, 10.1038/s41591-020-0805-8 · DOI · Paper page
  59. Chalabi, 2022, LBA7 neoadjuvant immune checkpoint inhibition in locally advanced MMR-deficient colon cancer: The NICHE-2 study, Ann Oncol, 33, S1389, 10.1016/j.annonc.2022.08.016 · DOI
  60. Lim, 2022, Phase III trial of chemoradiotherapy with temozolomide plus nivolumab or placebo for newly diagnosed glioblastoma with methylated MGMT promoter, Neuro Oncol, 24, 1935, 10.1093/neuonc/noac116 · DOI
  61. Brahm, 2020, The current status of immune checkpoint inhibitors in neuro-oncology: A systematic review, Cancers (Basel), 12, 10.3390/cancers12030586 · DOI
  62. Wang, 2021, Immunotherapy for recurrent glioblastoma: practical insights and challenging prospects, Cell Death Disease., 12, 299, 10.1038/s41419-021-03568-0 · DOI
  63. Lee, 2021, Neoadjuvant PD-1 blockade induces T cell and cDC1 activation but fails to overcome the immunosuppressive tumor associated macrophages in recurrent glioblastoma, Nat Commun, 12, 6938, 10.1038/s41467-021-26940-2 · DOI
  64. Niesel, 2021, The immune suppressive microenvironment affects efficacy of radio-immunotherapy in brain metastasis, EMBO Mol Med, 13, 10.15252/emmm.202013412 · DOI
  65. Lin, 2022, The role of myeloid cells in GBM immunosuppression, Front Immunol, 13, 10.3389/fimmu.2022.887781 · DOI
  66. Gross, 2022, Neoadjuvant cemiplimab for stage II to IV cutaneous squamous-cell carcinoma, N Engl J Med, 387, 10.1056/NEJMoa2209813 · DOI
  67. Frederico, 2022, 222 developing an adoptive cell transfer immunotherapy for pediatric high-grade gliomas, J ImmunoTherapy Cancer., 10, 10.1136/jitc-2022-SITC2022.0222 · DOI
  68. Penas-Prado, 2021, CTIM-32. Immune checkpoint inhibitor nivolumab in people with recurrent select rare cns cancers: Results of interim analysis in a heavily pretreated cohort, Neuro Oncol, 23, 10.1093/neuonc/noab196.224 · DOI
  69. Chongsathidkiet, 2018, Sequestration of T cells in bone marrow in the setting of glioblastoma and other intracranial tumors, Nat Med, 24, 10.1038/s41591-018-0135-2 · DOI
  70. O'Donnell, 2019, The promise of neoadjuvant immunotherapy and surgery for cancer treatment, Clin Cancer Res, 25, 10.1158/1078-0432.CCR-18-2641 · DOI
  71. Ahern, 2021, Neoadjuvant immunotherapy for non-small cell lung cancer: right drugs, right patient, right time, J Immunother Cancer., 9, 10.1136/jitc-2020-002248 · DOI
  72. Bilusic, 2022, What are the advantages of neoadjuvant immunotherapy over adjuvant immunotherapy, Expert Rev Anticancer Ther, 22, 10.1080/14737140.2022.2069097 · DOI
  73. Hogan, 2011, Surgery induced immunosuppression, Surgeon, 9, 38, 10.1016/j.surge.2010.07.011 · DOI

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Metadata

Authors
Frederico, S. C., Darling, C., Bielanin, J. P., Dubinsky, A. C., Zhang, X., Hadjipanayis, C. G., & Kohanbash, G.
Venue
Frontiers in Immunology
Publisher
Frontiers Media SA
Published
2023-02-17
Volume
14
ISSN
1664-3224
DOI
10.3389/fimmu.2023.1057567
PMC
PMC9981631
Cited by
15
References
12
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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