Changes in clinical management of diffuse IDH-mutated lower-grade gliomas: patterns of care in a 15-year period.
Brain neoplasm
Low-grade glioma
Neurosurgery
Treatment outcome
Journal
Journal of neuro-oncology
ISSN: 1573-7373
Titre abrégé: J Neurooncol
Pays: United States
ID NLM: 8309335
Informations de publication
Date de publication:
Dec 2022
Dec 2022
Historique:
received:
19
08
2022
accepted:
14
09
2022
pubmed:
27
11
2022
medline:
21
12
2022
entrez:
26
11
2022
Statut:
ppublish
Résumé
Isocitrate dehydrogenase (IDH) mutated diffuse lower-grade gliomas (dLGG) are infiltrating brain tumors and increasing evidence is in favor of early multimodal treatment. In a Scandinavian population-based setting, we wanted to study treatment patterns over the last 15 years, focusing on the short-term postoperative course to better understand the potential negative consequences of treatment. Patients ≥ 18 years with primary IDH-mutated dLGG grade 2 and 3, operated between January 2007-June 2021 were identified. Patients were divided into subgroups (2007-2011, 2012-2016, and 2017-2021) and comparisons regarding tumor- and disease characteristics, treatment, and postoperative outcome were performed. We identified 202 patients (n = 61, 2007-2011; n = 72, 2012-2016; n = 69, 2017-2021), where of 193 underwent resection without change in proportion of resections over time. More patients underwent complete resections in recent times (6.1%; 15.7%; 26.1%, respectively; p = 0.016). Forty-two patients had any neurological deficit postoperatively (14.8%; 23.6%; 23.2%; p = 0.379), mostly minor and transient. Differences in oncological therapy were seen between the investigated subgroups. Early radiotherapy alone (32.8%; 7%; 2.9%; p < 0.001), concomitant chemoradiotherapy (23%; 37.5%; 17.4%; p = 0.022), sequential chemoradiotherapy (0%; 18%; 49.3%; p < 0.001), and no adjuvant treatment (42.6%; 23.6%; 18.8%; p = 0.009) shifted during the studied period. Increasingly more patients received proton radiotherapy compared to photon radiotherapy during the later time periods (p < 0.001). Complete resections were performed more often in later time periods without an apparent increase in surgical morbidity. Early adjuvant oncological treatment shifted towards providing chemotherapy and combined chemoradiotherapy more often in later time periods. Protons replaced photons as the radiation modality of choice.
Sections du résumé
BACKGROUND
BACKGROUND
Isocitrate dehydrogenase (IDH) mutated diffuse lower-grade gliomas (dLGG) are infiltrating brain tumors and increasing evidence is in favor of early multimodal treatment. In a Scandinavian population-based setting, we wanted to study treatment patterns over the last 15 years, focusing on the short-term postoperative course to better understand the potential negative consequences of treatment.
METHODS
METHODS
Patients ≥ 18 years with primary IDH-mutated dLGG grade 2 and 3, operated between January 2007-June 2021 were identified. Patients were divided into subgroups (2007-2011, 2012-2016, and 2017-2021) and comparisons regarding tumor- and disease characteristics, treatment, and postoperative outcome were performed.
RESULTS
RESULTS
We identified 202 patients (n = 61, 2007-2011; n = 72, 2012-2016; n = 69, 2017-2021), where of 193 underwent resection without change in proportion of resections over time. More patients underwent complete resections in recent times (6.1%; 15.7%; 26.1%, respectively; p = 0.016). Forty-two patients had any neurological deficit postoperatively (14.8%; 23.6%; 23.2%; p = 0.379), mostly minor and transient. Differences in oncological therapy were seen between the investigated subgroups. Early radiotherapy alone (32.8%; 7%; 2.9%; p < 0.001), concomitant chemoradiotherapy (23%; 37.5%; 17.4%; p = 0.022), sequential chemoradiotherapy (0%; 18%; 49.3%; p < 0.001), and no adjuvant treatment (42.6%; 23.6%; 18.8%; p = 0.009) shifted during the studied period. Increasingly more patients received proton radiotherapy compared to photon radiotherapy during the later time periods (p < 0.001).
CONCLUSION
CONCLUSIONS
Complete resections were performed more often in later time periods without an apparent increase in surgical morbidity. Early adjuvant oncological treatment shifted towards providing chemotherapy and combined chemoradiotherapy more often in later time periods. Protons replaced photons as the radiation modality of choice.
Identifiants
pubmed: 36434487
doi: 10.1007/s11060-022-04136-y
pii: 10.1007/s11060-022-04136-y
pmc: PMC9758083
doi:
Substances chimiques
Isocitrate Dehydrogenase
EC 1.1.1.41
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
535-543Subventions
Organisme : Agreement between the Swedish government and the country councils, the ALF-agreement
ID : ALFGBG-716671
Organisme : Vetenskapsrådet
ID : 2017-00944
Informations de copyright
© 2022. The Author(s).
Références
Ostrom QT, Gittleman H, Fulop J et al (2015) CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2008–2012. Neuro-oncology 17(Suppl 4):iv1–iv62
doi: 10.1093/neuonc/nov189
Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO Classification of Tumors of the Central Nervous System: a summary. Neuro Oncol. 23:1231–1251
Eckel-Passow JE, Lachance DH, Molinaro AM et al (2015) Glioma Groups Based on 1p/19q, IDH, and TERT Promoter Mutations in Tumors. N Engl J Med 372(26):2499–2508
doi: 10.1056/NEJMoa1407279
Cancer Genome Atlas Research N, Brat DJ, Verhaak RG et al (2015) Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas. N Engl J Med 372(26):2481–2498
doi: 10.1056/NEJMoa1402121
Jakola AS, Skjulsvik AJ, Myrmel KS et al (2017) Surgical resection versus watchful waiting in low-grade gliomas. Ann Oncol 28(8):1942–1948
doi: 10.1093/annonc/mdx230
Patel SH, Bansal AG, Young EB et al (2019) Extent of Surgical Resection in Lower-Grade Gliomas: Differential Impact Based on Molecular Subtype. AJNR Am J Neuroradiol 40(7):1149–1155
doi: 10.3174/ajnr.A6102
Wijnenga MMJ, French PJ, Dubbink HJ et al (2018) The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological, and molecular analysis. Neuro-oncology 20(1):103–112
doi: 10.1093/neuonc/nox176
Still MEH, Roux A, Huberfeld G et al (2019) Extent of Resection and Residual Tumor Thresholds for Postoperative Total Seizure Freedom in Epileptic Adult Patients Harboring a Supratentorial Diffuse Low-Grade Glioma. Neurosurgery 85(2):E332–E340
doi: 10.1093/neuros/nyy481
Ius T, Pauletto G, Tomasino B et al (2020) Predictors of Postoperative Seizure Outcome in Low Grade Glioma: From Volumetric Analysis to Molecular Stratification. Cancers (Basel): 12(2):397
Weller M, van den Bent M, Preusser M et al (2021) EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol 18(3):170–186
doi: 10.1038/s41571-020-00447-z
Buckner J, Giannini C, Eckel-Passow J et al (2017) Management of diffuse low-grade gliomas in adults - use of molecular diagnostics. Nat Rev Neurol 13(6):340–351
doi: 10.1038/nrneurol.2017.54
Buckner JC, Shaw EG, Pugh SL et al (2016) Radiation plus Procarbazine, CCNU, and Vincristine in Low-Grade Glioma. N Engl J Med 374(14):1344–1355
doi: 10.1056/NEJMoa1500925
van den Bent MJ, Brandes AA, Taphoorn MJ et al (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin oncology: official J Am Soc Clin Oncol 31(3):344–350
doi: 10.1200/JCO.2012.43.2229
Cairncross JG, Wang M, Jenkins RB et al (2014) Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J Clin oncology: official J Am Soc Clin Oncol 32(8):783–790
doi: 10.1200/JCO.2013.49.3726
Carstam L, Smits A, Milos P et al (2019) Neurosurgical patterns of care for diffuse low-grade gliomas in Sweden between 2005 and 2015. Neurooncol Pract 6(2):124–133
Solheim O, Jakola AS, Gulati S, Johannesen TB (2012) Incidence and causes of perioperative mortality after primary surgery for intracranial tumors: a national, population-based study. J Neurosurg 116(4):825–834
doi: 10.3171/2011.12.JNS11339
De Witt Hamer PC, De Witt Hamer PC, Klein M, Hervey-Jumper SL, Wefel JS, Berger MS (2021) Functional Outcomes and Health-Related Quality of Life Following Glioma Surgery. Neurosurgery 88(4):720–732
doi: 10.1093/neuros/nyaa365
De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin oncology: official J Am Soc Clin Oncol 30(20):2559–2565
doi: 10.1200/JCO.2011.38.4818
Pignatti F, van den Bent M, Curran D et al (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin oncology: official J Am Soc Clin Oncol 20(8):2076–2084
doi: 10.1200/JCO.2002.08.121
Baumert BG, Hegi ME, van den Bent MJ et al (2016) Temozolomide chemotherapy versus radiotherapy in high-risk low-grade glioma (EORTC 22033–26033): a randomised, open-label, phase 3 intergroup study. Lancet Oncol 17(11):1521–1532
doi: 10.1016/S1470-2045(16)30313-8
Douw L, Klein M, Fagel SS et al (2009) Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8(9):810–818
doi: 10.1016/S1474-4422(09)70204-2
Jakola AS, Skjulsvik AJ, Myrmel KS et al (2017) Surgical resection versus watchful waiting in low-grade gliomas. Ann Oncol. 28(8):1942-1948
Jakola AS, Myrmel KS, Kloster R et al (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. Jama 308(18):1881–1888
doi: 10.1001/jama.2012.12807
Martin RC, Gerstenecker A, Nabors LB, Marson DC, Triebel KL (2015) Impairment of medical decisional capacity in relation to Karnofsky Performance Status in adults with malignant brain tumor. Neurooncol Pract 2(1):13–19
Compston A (2010) Aids to the investigation of peripheral nerve injuries. Medical Research Council: Nerve Injuries Research Committee. His Majesty’s Stationery Office: ; 1942;pp. 48 (iii) and 74 figures and 7 diagrams; with aids to the examination of the peripheral nervous system. By Michael O’Brien for the Guarantors of Brain. Saunders Elsevier: 2010; pp. [8] 64 and 94 Figures. Brain;133(10):2838–2844
Landriel Ibanez FA, Hem S, Ajler P et al (2011) A new classification of complications in neurosurgery. World Neurosurg 75(5–6):709–715 discussion 604–711
doi: 10.1016/j.wneu.2010.11.010
Fedorov A, Beichel R, Kalpathy-Cramer J et al (2012) 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson imaging 30(9):1323–1341
doi: 10.1016/j.mri.2012.05.001
Corell A, Ferreyra Vega S, Hoefling N et al (2020) The clinical significance of the T2-FLAIR mismatch sign in grade II and III gliomas: a population-based study. BMC Cancer 20(1):450
doi: 10.1186/s12885-020-06951-w
Ferreyra Vega S, Olsson Bontell T, Corell A, Smits A, Jakola AS, Carén H (2021) DNA methylation profiling for molecular classification of adult diffuse lower-grade gliomas. Clin Epigenetics 13(1):102
doi: 10.1186/s13148-021-01085-7
Jakola AS, Pedersen LK, Skjulsvik AJ, Myrmel K, Sjavik K, Solheim O (2022) The impact of resection in IDH-mutant WHO grade 2 gliomas: a retrospective population-based parallel cohort study. J Neurosurg. 137(5):1321–1328
Delev D, Heiland DH, Franco P et al (2019) Surgical management of lower-grade glioma in the spotlight of the 2016 WHO classification system. J Neurooncol 141(1):223–233
doi: 10.1007/s11060-018-03030-w
Vassal M, Charroud C, Deverdun J et al (2017) Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. J Neurosurg 126(4):1181–1190
doi: 10.3171/2016.4.JNS152484
Duffau H, Capelle L, Denvil D et al (2003) Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74(7):901–907
doi: 10.1136/jnnp.74.7.901
Bo HK, Solheim O, Kvistad KA et al (2019) Intraoperative 3D ultrasound-guided resection of diffuse low-grade gliomas: radiological and clinical results. J Neurosurg 132(2):518–529
doi: 10.3171/2018.10.JNS181290
Berger A, Tzarfati G, Costa M et al (2019) Incidence and impact of stroke following surgery for low-grade gliomas. J Neurosurg.:134(1):153–161
Dhermain F, Barani IJ (2016) Complications from radiotherapy. Handb Clin Neurol 134:219–234
doi: 10.1016/B978-0-12-802997-8.00013-X
Shaw EG, Wang M, Coons SW et al (2012) Randomized trial of radiation therapy plus procarbazine, lomustine, and vincristine chemotherapy for supratentorial adult low-grade glioma: initial results of RTOG 9802. J Clin oncology: official J Am Soc Clin Oncol 30(25):3065–3070
doi: 10.1200/JCO.2011.35.8598
Pignatti F, van den Bent M, Curran D et al (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20(8):2076–2084
doi: 10.1200/JCO.2002.08.121
Chang EF, Smith JS, Chang SM et al (2008) Preoperative prognostic classification system for hemispheric low-grade gliomas in adults. J Neurosurg 109(5):817–824
doi: 10.3171/JNS/2008/109/11/0817
Etxaniz O, Carrato C, de Aguirre I et al (2017) IDH mutation status trumps the Pignatti risk score as a prognostic marker in low-grade gliomas. J Neurooncol 135(2):273–284
doi: 10.1007/s11060-017-2570-1
Tabrizi S, Yeap BY, Sherman JC et al (2019) Long-term outcomes and late adverse effects of a prospective study on proton radiotherapy for patients with low-grade glioma. Radiother Oncol 137:95–101
doi: 10.1016/j.radonc.2019.04.027