Progression-free survival versus post-progression survival and overall survival in WHO grade 2 gliomas
DOI:
https://doi.org/10.2340/1651-226X.2024.40845Keywords:
Brain Neoplasms, Surrogate endpoints, Response assessment criteria, Prognostic factors, OncologyAbstract
Background and purpose: Progression-free survival (PFS) remains to be validated as an outcome measure for diffuse WHO grade 2 gliomas, and knowledge about the relationships between PFS, post-progression survival (PPS), and overall survival (OS) in this subset of tumors is limited. We sought to assess correlations between PFS and OS, and identify factors associated with PFS, PPS, and OS in patients treated for diffuse supratentorial WHO grade 2 gliomas.
Material and methods: We included 319 patients from three independent observational cohorts. The correlation between PFS and OS was analyzed using independent exponential distributions for PFS and time from progression to death. Cox proportional hazards models were used to determine the effects of covariates on PFS, PPS, and OS.
Results: The overall correlation between PFS and OS was rs0.31. The correlation was rs 0.37 for astrocytomas and rs 0.19 for oligodendrogliomas. Longer PFS did not predict longer PPS. Patients with astrocytomas had shorter PFS, PPS, and OS. Larger preoperative tumor volume was a risk factor for shorter PFS, while older age was a risk factor for shorter PPS and OS. Patients who received early radio- and chemotherapy had longer PFS, but shorter PPS and OS.
Interpretation: We found a weak correlation between PFS and OS in WHO grade 2 gliomas, with the weakest correlation observed in oligodendrogliomas. Our analyses did not demonstrate any association between PFS and PPS. Critically, predictors of PFS are not necessarily predictors of OS. There is a need for validation of PFS as an endpoint in diffuse WHO grade 2 gliomas.
Downloads
References
Jakola AS, Skjulsvik AJ, Myrmel KS, Sjavik K, Unsgard G, Torp SH, et al. Surgical resection versus watchful waiting in low-grade gliomas. Ann Oncol. 2017;28(8):1942–8.
https://doi.org/10.1093/annonc/mdx230 DOI: https://doi.org/10.1093/annonc/mdx230
Hervey-Jumper SL, Zhang Y, Phillips JJ, Morshed RA, Young JS, McCoy L, et al. Interactive effects of molecular, therapeutic, and patient factors on outcome of diffuse low-grade glioma. J Clin Oncol. 2023;41(11):2029–42.
https://doi.org/10.1200/JCO.21.02929 DOI: https://doi.org/10.1200/JCO.21.02929
Mellinghoff IK, van den Bent MJ, Blumenthal DT, Touat M, Peters KB, Clarke J, et al. Vorasidenib in IDH1- or IDH2-mutant low-grade glioma. N Engl J Med. 2023;389(7):589–601.
https://doi.org/10.1056/NEJMoa2304194 DOI: https://doi.org/10.1056/NEJMoa2304194
Prentice RL. Surrogate endpoints in clinical trials: definition and operational criteria. Stat Med. 1989;8(4):431–40.
https://doi.org/10.1002/sim.4780080407 DOI: https://doi.org/10.1002/sim.4780080407
Amir E, Seruga B, Kwong R, Tannock IF, Ocaña A. Poor correlation between progression-free and overall survival in modern clinical trials: are composite endpoints the answer? Eur J Cancer. 2012;48(3):385–8.
https://doi.org/10.1016/j.ejca.2011.10.028 DOI: https://doi.org/10.1016/j.ejca.2011.10.028
Han K, Ren M, Wick W, Abrey L, Das A, Jin J, et al. Progression-free survival as a surrogate endpoint for overall survival in glioblastoma: a literature-based meta-analysis from 91 trials. Neuro Oncol. 2014;16(5):696–706. DOI: https://doi.org/10.1093/neuonc/not236
Ballman KV, Buckner JC, Brown PD, Giannini C, Flynn PJ, LaPlant BR, et al. The relation-ship between six-month progression-free survival and 12-month overall sur-vival end points for phase II trials in patients with glioblastoma multiforme. Neuro Oncol. 2007;9(1):29–38.
https://doi.org/10.1215/15228517-2006-025 DOI: https://doi.org/10.1215/15228517-2006-025
Polley MY, Lamborn KR, Chang SM, Butowski N, Clarke JL, Prados M. Six-month progres-sion-free survival as an alternative primary efficacy endpoint to overall survival in newly diagnosed glioblastoma patients receiving temozolomide. Neuro Oncol. 2010;12(3):274–82.
https://doi.org/10.1093/neuonc/nop034 DOI: https://doi.org/10.1093/neuonc/nop034
van den Bent MJ, Afra D, de Witte O, Ben Hassel M, Schraub S, Hoang-Xuan K, et al. Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet. 2005;366(9490):985–90.
https://doi.org/10.1016/S0140-6736(05)67070-5 DOI: https://doi.org/10.1016/S0140-6736(05)67070-5
US Food and Drugs Administration. Clinical trial endpoints for the approval of cancer drugs and biologics. US Food and Drug administration (2018). (Cited date: 02.10.2024) https://www.fda.gov/media/71195/download
Wen PY, Chang SM, Van den Bent MJ, Vogelbaum MA, Macdonald DR, Lee EQ. Response assessment in neuro-oncology clinical trials. J Clin Oncol. 2017;35(21):2439–49. DOI: https://doi.org/10.1200/JCO.2017.72.7511
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 On-col. 2021;23(8):1231–51.
https://doi.org/10.1093/neuonc/noab106 DOI: https://doi.org/10.1093/neuonc/noab106
Jakola AS, Pedersen LK, Skjulsvik AJ, Myrmel K, Sjåvik K, Solheim O. The impact of resec-tion in IDH-mutant WHO grade 2 gliomas: a retrospective population-based parallel cohort study. J. Neurosurg. 2022 Mar 4;137(5):1321-1328.
https://doi.org/10.3171/2022.1.JNS212514 DOI: https://doi.org/10.3171/2022.1.JNS212514
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.
https://doi.org/10.1634/theoncologist.2009-0121 DOI: https://doi.org/10.1634/theoncologist.2009-0121
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.
https://doi.org/10.1056/NEJMoa1308573 DOI: https://doi.org/10.1056/NEJMoa1308573
Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):709–22. DOI: https://doi.org/10.1056/NEJMoa1308345
Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgård G, et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful wait-ing in low-grade gliomas. JAMA. 2012;308(18):1881–8. DOI: https://doi.org/10.1001/jama.2012.12807
Huang RY, Young RJ, Ellingson BM, Veeraraghavan H, Wang W, Tixier F, et al. Volumetric analysis of IDH-mutant lower-grade glioma: a natural history study of tumor growth rates before and after treatment. Neuro Oncol. 2020;22(12):1822–30.
https://doi.org/10.1093/neuonc/noaa105 DOI: https://doi.org/10.1093/neuonc/noaa105
Pallud J, Taillandier L, Capelle L, Fontaine D, Peyre M, Ducray F, et al. Quantitative morpho-logical magnetic resonance imaging follow-up of low-grade glioma: a plea for systematic measurement of growth rates. Neurosurgery. 2012;71(3):729–39; discussion 39–40.
https://doi.org/10.1227/NEU.0b013e31826213de DOI: https://doi.org/10.1227/NEU.0b013e31826213de
Alattar AA, Brandel MG, Hirshman BR, Dong X, Carroll KT, Ali MA, et al. Oligodendroglioma resection: a Surveillance, Epidemiology, and End Results (SEER) analysis. J Neurosurg. 2018;128(4):1076–83.
https://doi.org/10.3171/2016.11.JNS161974 DOI: https://doi.org/10.3171/2016.11.JNS161974
Bell EH, Zhang P, Shaw EG, Buckner JC, Barger GR, Bullard DE, et al. Comprehensive ge-nomic analysis in NRG Oncology/RTOG 9802: a phase III trial of radiation ver-sus radiation plus procarbazine, lomustine (CCNU), and vincristine in high-risk low-grade glioma. J Clin Oncol. 2020;38(29):3407–17. DOI: https://doi.org/10.1200/JCO.19.02983
Buckner JC, Shaw EG, Pugh SL, Chakravarti A, Gilbert MR, Barger GR, et al. Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med. 2016;374(14):1344–55. DOI: https://doi.org/10.1056/NEJMoa1500925
Gui C, Kosteniuk SE, Lau JC, Megyesi JF. Tumor growth dynamics in serially-imaged low-grade glioma patients. J Neurooncol. 2018;139(1):167–75.
https://doi.org/10.1007/s11060-018-2857-x DOI: https://doi.org/10.1007/s11060-018-2857-x
Bosma I, Reijneveld JC, Douw L, Vos MJ, Postma TJ, Aaronson NK, et al. Health-related quality of life of long-term high-grade glioma survivors. Neuro Oncol. 2009;11(1):51–8.
https://doi.org/10.1215/15228517-2008-049 DOI: https://doi.org/10.1215/15228517-2008-049
Yavas C, Zorlu F, Ozyigit G, Gurkaynak M, Yavas G, Yuce D, et al. Health-related quality of life in high-grade glioma patients: a prospective single-center study. Support Care Cancer. 2012;20(10):2315–25.
https://doi.org/10.1007/s00520-011-1340-4 DOI: https://doi.org/10.1007/s00520-011-1340-4
Osoba D, Brada M, Yung W, Prados M. Health-related quality of life in patients treated with temozolomide versus procarbazine for recurrent glioblastoma multiforme. J Clin Oncol. 2000;18(7):1481–91. DOI: https://doi.org/10.1200/JCO.2000.18.7.1481
Dirven L, van den Bent MJ, Bottomley A, van der Meer N, van der Holt B, Vos MJ, et al. The impact of bevacizumab on health-related quality of life in patients treated for recurrent glioblastoma: results of the randomised controlled phase 2 BELOB trial. Eur J Cancer. 2015;51(10):1321–30. DOI: https://doi.org/10.1016/j.ejca.2015.03.025
Dirven L, Reijneveld JC, Taphoorn MJB, Coens C, El-Badawy SA, Tzuk-Shina T, et al. Impact of radiation target volume on health-related quality of life in patients with low-grade glioma in the 2-year period post treatment: a secondary analysis of the EORTC 22033–26033. Int J Radiat Oncol Biol Phys. 2019;104(1):90–100. DOI: https://doi.org/10.1016/j.ijrobp.2019.01.003
Coomans MB, Dirven L, Aaronson N, Baumert BG, van den Bent M, Bottomley A, et al. Fac-tors associated with health-related quality of life (HRQoL) deterioration in gli-oma patients during the progression-free survival period. Neuro Oncol. 2022;24(12):2159–69.
https://doi.org/10.1093/neuonc/noac097 DOI: https://doi.org/10.1093/neuonc/noac097
Koekkoek JAF, Kerkhof M, Dirven L, Heimans JJ, Reijneveld JC, Taphoorn MJB. Seizure out-come after radiotherapy and chemotherapy in low-grade glioma patients: a systematic review. Neuro Oncol. 2015;17(7):924–34.
https://doi.org/10.1093/neuonc/nov032 DOI: https://doi.org/10.1093/neuonc/nov032
Avila EK, Chamberlain M, Schiff D, Reijneveld JC, Armstrong TS, Ruda R, et al. Seizure con-trol as a new metric in assessing efficacy of tumor treatment in low-grade gli-oma trials. Neuro Oncol. 2017;19(1):12–21.
https://doi.org/10.1093/neuonc/now190 DOI: https://doi.org/10.1093/neuonc/now190
Provenzale JM, Ison C, Delong D. Bidimensional measurements in brain tumors: assess-ment of interobserver variability. Am J Roentgenol. 2009;193(6):W515–22. DOI: https://doi.org/10.2214/AJR.09.2615
van den Bent MJ, Wefel JS, Schiff D, Taphoorn MJ, Jaeckle K, Junck L, et al. Response as-sessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol. 2011;12(6):583–93.
https://doi.org/10.1016/S1470-2045(11)70057-2 DOI: https://doi.org/10.1016/S1470-2045(11)70057-2
Ritterbusch R, Halasz LM, Graber JJ. Distinct imaging patterns of pseudoprogression in glioma patients following proton versus photon radiation therapy. J Neuro-Oncol. 2021;152(3):583–90.
https://doi.org/10.1007/s11060-021-03734-6 DOI: https://doi.org/10.1007/s11060-021-03734-6
Wen PY, van den Bent M, Youssef G, Cloughesy TF, Ellingson BM, Weller M, et al. RANO 2.0: Update to the response assessment in neuro-oncology criteria for high- and low-grade gliomas in adults. J Clin Oncol. 2023;41(33):5187–99.
https://doi.org/10.1200/JCO.23.01059 DOI: https://doi.org/10.1200/JCO.23.01059
Additional Files
Published
How to Cite
Issue
Section
Categories
License
Copyright (c) 2023 Lisa Millgård Sagberg, Øyvind Salvesen, Asgeir Store Jakola, Erik Thurin, Eddie de Dios, Noah L.A. Nawabi, John L. Kilgallon, Joshua D. Bernstock, Vasileios K. Kavouridis, Timothy R. Smith, Ole Solheim

This work is licensed under a Creative Commons Attribution 4.0 International License.
