Association of supratotal resection with progression-free survival, malignant transformation, and overall survival in lower-grade gliomas

Neuro-Oncology - Tập 23 Số 5 - Trang 812-826 - 2021
Marco Rossi1,2, Lorenzo Gay1,2, Federico Ambrogi3, Marco Conti Nibali1,2, Tommaso Sciortino1,2, Guglielmo Puglisi1,2, Antonella Leonetti1,2, Cristina Mocellini4, Manuela Caroli5, Susanna Cordera6, Matteo Simonelli7, Federico Pessina7, Pierina Navarria7, Andrea Pace8, Riccardo Soffietti9, Roberta Rudà9, Marco Riva1,2, Lorenzo Bello1,2
1IRCCS Istituto Ortopedico Galeazzi, Neurosurgical Oncology Unit, Milano, Italy
2Neurosurgical Oncology Unit, Dept of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milano, Italy
3Laboratory of Medical Statistics, Biometry and Epidemiology “G.A.Maccararo,” Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milano, Italy
4Neuro-oncologia, Divisione di Neurologia, Ospedale Santa Croce e Carle, Cuneo, Italy
5Neurochirurgia, Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Milano, Italy
6Neuro-oncologia, Divisione di Neurologia, Ospedale Regionale Parini, Aosta, Italy
7Humanitas Cancer Center, Humanitas Research Hospital, IRCCS, Rozzano, Italy
8Neuro-Oncologia, Istituto Nazionale Tumori Regina Elena, Roma, Italy
9Neuro-Oncologia, Città della Salute e della Scienza, Università di Torino, Torino, Italy

Tóm tắt

Abstract Background Supratotal resection is advocated in lower-grade gliomas (LGGs) based on theoretical advantages but with limited verification of functional risk and data on oncological outcomes. We assessed the association of supratotal resection in molecularly defined LGGs with oncological outcomes. Methods Included were 460 presumptive LGGs; 404 resected; 347 were LGGs, 319 isocitrate dehydrogenase (IDH)–mutated, 28 wildtype. All patients had clinical, imaging, and molecular data. Resection aimed at supratotal resection without any patient or tumor a priori selection. The association of extent of resection (EOR), categorized on volumetric fluid attenuated inversion recovery images as residual tumor volume, along with postsurgical management with progression-free survival (PFS), malignant (M)PFS, and overall survival (OS) assessed by univariate, multivariate, and propensity score analysis. The study mainly focused on IDH-mutated LGGs, the “typical LGGs.” Results Median follow-up was 6.8 years (interquartile range, 5–8). Out of 319 IDH-mutated LGGs, 190 (59.6%) progressed, median PFS: 4.7 years (95% CI: 4–5.3). Total and supratotal resection obtained in 39% and 35% of patients with IDH1-mutated tumors. In IDH-mutated tumors, most patients in the partial/subtotal group progressed, 82.4% in total, only 6 (5.4%) in supratotal. Median PFS was 29 months (95% CI: 25–36) in subtotal, 46 months (95% CI: 38–48) in total, while at 92 months, PFS in supratotal was 94.0%. There was no association with molecular subtypes and grade. At random forest analysis, PFS strongly associated with EOR, radiotherapy, and previous treatment. In the propensity score analysis, EOR associated with PFS (hazard ratio, 0.03; 95% CI: 0.01–0.13). MPFS occurred in 32.1% of subtotal total groups; 1 event in supratotal. EOR, grade III, previous treatment correlated to MPFS. At random forest analysis, OS associated with EOR as well. Conclusions Supratotal resection strongly associated with PFS, MPFS, and OS in LGGs, regardless of molecular subtypes and grade, right from the beginning of clinical presentation.

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Tài liệu tham khảo

Reuss, 2015, IDH mutant diffuse and anaplastic astrocytomas have similar age at presentation and little difference in survival: a grading problem for WHO, Acta Neuropathol., 129, 867, 10.1007/s00401-015-1438-8

Buckner, 2017, Management of diffuse low-grade gliomas in adults—use of molecular diagnostics, Nat Rev Neurol., 13, 340, 10.1038/nrneurol.2017.54

Schiff, 2019, Recent developments and future directions in adult lower-grade gliomas: Society for Neuro-Oncology (SNO) and European Association of Neuro-Oncology (EANO) consensus, Neuro Oncol., 21, 837, 10.1093/neuonc/noz033

Jakola, 2012, Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas, JAMA., 308, 1881, 10.1001/jama.2012.12807

Jakola, 2017, Surgical resection versus watchful waiting in low-grade gliomas, Ann Oncol., 28, 1942, 10.1093/annonc/mdx230

Smith, 2008, Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas, J Clin Oncol., 26, 1338, 10.1200/JCO.2007.13.9337

Wijnenga, 2018, The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological, and molecular analysis, Neuro Oncol., 20, 103, 10.1093/neuonc/nox176

Rudà, 2020, Italian consensus and recommendations on diagnosis and treatment of low-grade gliomas. An intersociety (SINch/AINO/SIN) document, J Neurosurg Sci., 64, 313, 10.23736/S0390-5616.20.04982-6

Aghi, 2015, The role of surgery in the management of patients with diffuse low grade glioma: a systematic review and evidence-based clinical practice guideline, J Neurooncol., 125, 503, 10.1007/s11060-015-1867-1

Duffau, 2013, A new philosophy in surgery for diffuse low-grade glioma (DLGG): oncological and functional outcomes, Neurochirurgie., 59, 2, 10.1016/j.neuchi.2012.11.001

De Witt Hamer, 2012, Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis, J Clin Oncol., 30, 2559, 10.1200/JCO.2011.38.4818

Bello, 2014, Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways, Neuro Oncol., 16, 1110, 10.1093/neuonc/not327

Bello, 2010, Present day’s standards in microsurgery of low-grade gliomas, Adv Tech Stand Neurosurg., 35, 113, 10.1007/978-3-211-99481-8_5

Rossi, 2019, Is supratotal resection achievable in low-grade gliomas? Feasibility, putative factors, safety, and functional outcome, J Neurosurg, 17, 1

Yordanova, 2011, Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. Clinical article, J Neurosurg., 115, 232, 10.3171/2011.3.JNS101333

Pallud, 2010, Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities, Neurology., 74, 1724, 10.1212/WNL.0b013e3181e04264

Duffau, 2016, Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up, Acta Neurochir (Wien)., 158, 51, 10.1007/s00701-015-2621-3

Rossi, 2019, Mapping in low-grade glioma surgery: low- and high-frequency stimulation, Neurosurg Clin N Am., 30, 55, 10.1016/j.nec.2018.08.003

van den Bent, 2011, Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas, Lancet Oncol., 12, 583, 10.1016/S1470-2045(11)70057-2

Wen, 2017, Response assessment in neuro-oncology clinical trials, J Clin Oncol., 35, 2439, 10.1200/JCO.2017.72.7511

Weller, 2015, Molecular classification of diffuse cerebral WHO grade II/III gliomas using genome- and transcriptome-wide profiling improves stratification of prognostically distinct patient groups, Acta Neuropathol., 129, 679, 10.1007/s00401-015-1409-0

Choi, 2020, Extent of resection and molecular pathologic subtype are potent prognostic factors of adult WHO grade II glioma, Sci Rep, 10, 2086, 10.1038/s41598-020-59089-x

Sanai, 2011, Low-grade gliomas in adults, J Neurosurg., 115, 948, 10.3171/2011.7.JNS101238

Capelle, 2013, Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article, J Neurosurg., 118, 1157, 10.3171/2013.1.JNS121

Tom, 2019, Management for different glioma subtypes: are all low-grade gliomas created equal?, Am Soc Clin Oncol Educ Book., 39, 133, 10.1200/EDBK_238353