Functional and oncological outcomes following more than three consecutive surgical resections for multiple relapses of initially grade 2 IDH-mutated gliomas.
Awake mapping
Functional outcomes
Low-grade glioma
Relapse
Reoperation
Survival
Journal
Acta neurochirurgica
ISSN: 0942-0940
Titre abrégé: Acta Neurochir (Wien)
Pays: Austria
ID NLM: 0151000
Informations de publication
Date de publication:
28 Oct 2024
28 Oct 2024
Historique:
received:
10
08
2024
accepted:
16
10
2024
medline:
28
10
2024
pubmed:
28
10
2024
entrez:
28
10
2024
Statut:
epublish
Résumé
Second and third surgeries were demonstrated as safe and efficient in recurrent diffuse low-grade glioma (LGG). Here, the feasibility of more than 3 resections is investigated. Patients who underwent 4 or 5 operations for recurrent initially WHO grade 2 IDH-mutated gliomas were consecutively selected. Twenty-three operations were performed in five patients (all males, mean age 27.2 ± 4 years). Three patients underwent 5 surgeries and two patients underwent 4 surgeries. Twelve procedures (52%) were achieved with awake mapping, including all 4th and 5th operations but one. Repeat electrical mapping detected changes of the cortical maps between at least two awake surgeries in 4 patients. No patients experienced permanent neurological impairment (KPS score ≥ 80 in all cases). The patients returned to work after 22 surgeries among 23 (95.6%). There were 3 oligodendrogliomas and 2 astrocytomas (4 gliomas became malignant at fourth or fifth operation). Although the preoperative tumor volume significantly increased before the fourth (p = 0.026) and fifth operation (p = 0.003) compared with the first operation, there was no significant difference between the residual tumor volume after the fourth or fifth resection versus the first one. The mean delay was 10.6 ± 3.9 years before chemotherapy and 15.4 ± 3.4 years before radiotherapy (one patient never received adjuvant treatment after 21.5 years). The mean follow-up duration was 18.3 ± 3.1 years since the first surgery (2.3 ± 1.8 years since the last surgery). Three patients were still alive at last follow-up. This is the first series showing that to reoperate beyond three times is feasible with a low functional risk and a long survival in multiple LGG recurrences, with the use of awake mapping in 87.5% of 4th and 5th surgeries.
Sections du résumé
BACKGROUND
BACKGROUND
Second and third surgeries were demonstrated as safe and efficient in recurrent diffuse low-grade glioma (LGG). Here, the feasibility of more than 3 resections is investigated.
METHODS
METHODS
Patients who underwent 4 or 5 operations for recurrent initially WHO grade 2 IDH-mutated gliomas were consecutively selected.
RESULTS
RESULTS
Twenty-three operations were performed in five patients (all males, mean age 27.2 ± 4 years). Three patients underwent 5 surgeries and two patients underwent 4 surgeries. Twelve procedures (52%) were achieved with awake mapping, including all 4th and 5th operations but one. Repeat electrical mapping detected changes of the cortical maps between at least two awake surgeries in 4 patients. No patients experienced permanent neurological impairment (KPS score ≥ 80 in all cases). The patients returned to work after 22 surgeries among 23 (95.6%). There were 3 oligodendrogliomas and 2 astrocytomas (4 gliomas became malignant at fourth or fifth operation). Although the preoperative tumor volume significantly increased before the fourth (p = 0.026) and fifth operation (p = 0.003) compared with the first operation, there was no significant difference between the residual tumor volume after the fourth or fifth resection versus the first one. The mean delay was 10.6 ± 3.9 years before chemotherapy and 15.4 ± 3.4 years before radiotherapy (one patient never received adjuvant treatment after 21.5 years). The mean follow-up duration was 18.3 ± 3.1 years since the first surgery (2.3 ± 1.8 years since the last surgery). Three patients were still alive at last follow-up.
CONCLUSIONS
CONCLUSIONS
This is the first series showing that to reoperate beyond three times is feasible with a low functional risk and a long survival in multiple LGG recurrences, with the use of awake mapping in 87.5% of 4th and 5th surgeries.
Identifiants
pubmed: 39465448
doi: 10.1007/s00701-024-06321-6
pii: 10.1007/s00701-024-06321-6
doi:
Substances chimiques
Isocitrate Dehydrogenase
EC 1.1.1.41
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
425Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Alhalabi OT, Dao Trong P et al (2024) Repeat surgery of recurrent glioma for molecularly informed treatment in the age of precision oncology: a risk-benefit analysis. J Neurooncol 167(2):245–255. https://doi.org/10.1007/s11060-024-04595-5
doi: 10.1007/s11060-024-04595-5
pubmed: 38334907
pmcid: 11023957
Alvarez de Eulate-Beramendi S, Rigau V, Taillandier L, Duffau H (2014) Delayed leptomeningeal and subependymal seeding after multiple surgeries for supratentorial diffuse low-grade gliomas in adults. J Neurosurg 120:833–839. https://doi.org/10.3171/2013.10.JNS131512
doi: 10.3171/2013.10.JNS131512
pubmed: 24286144
Blonski M, Obara T, Brzenczek C et al (2022) Initial PCV chemotherapy followed by Radiotherapy is Associated with a prolonged response but late neurotoxicity in 20 diffuse low-Grade Glioma patients. Front Oncol 12:827897. https://doi.org/10.3389/fonc.2022.827897
doi: 10.3389/fonc.2022.827897
pubmed: 35311144
pmcid: 8931287
Boccuni L, Abellaneda-Pérez K, Martín-Fernández J et al (2023) Neuromodulation-induced prehabilitation to leverage neuroplasticity before brain tumor surgery: a single-cohort feasibility trial protocol. Front Neurol 2:1243857
doi: 10.3389/fneur.2023.1243857
Capelle L, Fontaine D, Mandonnet E et al (2013) Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases. J Neurosurg 118:1157–1168. https://doi.org/10.3171/2013.1.JNS121
doi: 10.3171/2013.1.JNS121
pubmed: 23495881
Capo G, Skrap M, Guarracino I et al (2020) Cognitive functions in repeated glioma surgery. Cancers (Basel) 12:1077. https://doi.org/10.3390/cancers12051077
doi: 10.3390/cancers12051077
pubmed: 32357421
Chaichana KL, McGirt MJ, Laterra J, Olivi A, Quiñones-Hinojosa A (2010) Recurrence and malignant degeneration after resection of adult hemispheric low-grade gliomas. J Neurosurg 112:10–17. https://doi.org/10.3171/2008.10.JNS08608
doi: 10.3171/2008.10.JNS08608
pubmed: 19361270
Darlix A, Deverdun J, Menjot de Champfleur N et al (2017) IDH mutation and 1p19q codeletion distinguish two radiological patterns of diffuse low-grade gliomas. J Neurooncol 133:37–45. https://doi.org/10.1007/s11060-017-2421-0
doi: 10.1007/s11060-017-2421-0
pubmed: 28434111
Darlix A, Rigau V, Fraisse J, Gozé C, Fabbro M, Duffau H (2020) Postoperative follow-up for selected diffuse low-grade gliomas with WHO grade III/IV foci. Neurology 94(8):e830–e841. https://doi.org/10.1212/WNL.0000000000008877
doi: 10.1212/WNL.0000000000008877
pubmed: 31969465
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 Oncol 30:2559–2565. https://doi.org/10.1200/JCO.2011.38.4818
doi: 10.1200/JCO.2011.38.4818
pubmed: 22529254
Di Perri D, Jmil S, Lawson TM et al (2023) Health-related quality of life and cognitive failures in patients with lower-grade gliomas treated with radiotherapy. Cancer Radiother 7:219–224. https://doi.org/10.1016/j.canrad.2022.10.004
doi: 10.1016/j.canrad.2022.10.004
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 8:810–818. https://doi.org/10.1016/S1474-4422(09)70204-2
doi: 10.1016/S1474-4422(09)70204-2
pubmed: 19665931
Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11:255–265
doi: 10.1038/nrneurol.2015.51
pubmed: 25848923
Duffau H (2016) Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir (Wien) 158:51–58. https://doi.org/10.1007/s00701-015-2621-32
doi: 10.1007/s00701-015-2621-32
pubmed: 26530708
Duffau H (2017) Diffuse Low-Grade Gliomas in Adults. 2nd ed. Duffau Ed, 2017. Springer International Publishing: Imprint: Springer. https://doi.org/10.1007/978-3-319-55466-2
Duffau H (2021) Brain connectomics applied to oncological neuroscience: from a traditional surgical strategy focusing on glioma topography to a meta-network approach. Acta Neurochir (Wien) 163:905–917. https://doi.org/10.1007/s00701-021-04752-z
doi: 10.1007/s00701-021-04752-z
pubmed: 33564906
Duffau H (2021) New Philosophy, clinical pearls, and methods for Intraoperative Cognition Mapping and monitoring à La Carte in Brain Tumor patients. Neurosurgery 88(5):919–930. https://doi.org/10.1093/neuros/nyaa363
doi: 10.1093/neuros/nyaa363
pubmed: 33463689
Duffau H (2021) Introducing the concept of brain metaplasticity in glioma: how to reorient the pattern of neural reconfiguration to optimize the therapeutic strategy. J Neurosurg 136:613–617. https://doi.org/10.3171/2021.5.JNS211214
doi: 10.3171/2021.5.JNS211214
pubmed: 34624858
Duffau H (2022) A personalized longitudinal strategy in low-Grade Glioma patients: predicting oncological and neural interindividual variability and its changes over years to think one step ahead. J Pers Med 12:1621. https://doi.org/10.3390/jpm12101621
doi: 10.3390/jpm12101621
pubmed: 36294760
pmcid: 9604939
Duffau H (2022) Repeated Awake Surgical Resection(s) for recurrent diffuse low-Grade gliomas: why, when, and how to reoperate? Front Oncol 12:947933. https://doi.org/10.3389/fonc.2022.947933
doi: 10.3389/fonc.2022.947933
pubmed: 35865482
pmcid: 9294369
Duffau H, Filippi M (2024) Moving towards a connectomic view of neuro-oncology. Lancet Neurol 23:655–656. https://doi.org/10.1016/S1474-4422(23)00291-0
doi: 10.1016/S1474-4422(23)00291-0
pubmed: 38876732
Ferracci FX, Michaud K, Duffau H (2019) The landscape of postsurgical recurrence patterns in diffuse low-grade gliomas. Crit Rev Oncol Hematol 138:148–155. https://doi.org/10.1016/j.critrevonc.2019.04.009
doi: 10.1016/j.critrevonc.2019.04.009
pubmed: 31092371
Fukuya Y, Ikuta S, Maruyama T et al (2019) Tumor recurrence patterns after surgical resection of intracranial low-grade gliomas. J Neurooncol 144:519–528. https://doi.org/10.1007/s11060-019-03250-8
doi: 10.1007/s11060-019-03250-8
pubmed: 31363908
Hamdan N, Duffau H (2022) Extending the multistage surgical strategy for recurrent initially low-grade gliomas: functional and oncological outcomes in 31 consecutive patients who underwent a third resection under awake mapping. J Neurosurg 136:1035–1044. https://doi.org/10.3171/2021.3.JNS21264
doi: 10.3171/2021.3.JNS21264
pubmed: 34507287
Herbet G, Maheu M, Costi E, Lafargue G, Duffau H (2016) Brain neuroplastic map mapping neuroplastic potential in brain-damaged patients. Brain 139:829–844. https://doi.org/10.1093/brain/awv394
doi: 10.1093/brain/awv394
pubmed: 26912646
Herbet G, Duffau H, Mandonnet E (2024) Predictors of cognition after glioma surgery: connectotomy, structure-function phenotype, plasticity. Brain 4:awae093. https://doi.org/10.1093/brain/awae093 . (Online ahead of print)
doi: 10.1093/brain/awae093
Hervey-Jumper SL, Zhang Y, Phillips JJ et al (2023) Interactive effects of Molecular, Therapeutic, and patient factors on outcome of diffuse low-Grade Glioma. J Clin Oncol 41:2029–2042. https://doi.org/10.1200/JCO.21.02929
doi: 10.1200/JCO.21.02929
pubmed: 36599113
pmcid: 10082290
Jakola AS, Bouget D, Reinertsen I et al (2020) Spatial distribution of malignant transformation in patients with low-grade glioma. J Neurooncol 146:373–380. https://doi.org/10.1007/s11060-020-03391-1
doi: 10.1007/s11060-020-03391-1
pubmed: 31915981
pmcid: 6971181
Latini F, Fahlström M, Hesselager G, Zetterling M, Ryttlefors M (2020) Differences in the preferential location and invasiveness of diffuse low-grade gliomas and their impact on outcome. Cancer Med 9:5446–5458. https://doi.org/10.1002/cam4.3216
doi: 10.1002/cam4.3216
pubmed: 32537906
pmcid: 7402839
Lemaitre AL, Herbet G, Ng S, Moritz-Gasser S, Duffau H (2022) Cognitive preservation following awake mapping-based neurosurgery for low-grade gliomas: a longitudinal, within-patient design study. Neuro-Oncol 24:781–793. https://doi.org/10.1093/neuonc/noab275
doi: 10.1093/neuonc/noab275
pubmed: 34850187
Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO classification of tumors of the Central Nervous System: a Summary. Neurooncology 23:1231–1251
Mandonnet E, Delattre J, Tanguy M et al (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53:524–528. https://doi.org/10.1002/ana.10528
doi: 10.1002/ana.10528
pubmed: 12666121
Mandonnet E, De Witt Hamer P, Poisson I et al (2015) Initial experience using awake surgery for glioma: oncological, functional, and employment outcomes in a consecutive series of 25 cases. Neurosurgery 76:382–389. https://doi.org/10.1227/NEU.0000000000000644 . (discussion 389)
doi: 10.1227/NEU.0000000000000644
pubmed: 25621981
Ng S, Duffau H (2023) Brain plasticity profiling as a key support to therapeutic decision-making in low-Grade Glioma Oncological Strategies. Cancers 15(14):3698. https://doi.org/10.3390/cancers15143698
doi: 10.3390/cancers15143698
pubmed: 37509359
pmcid: 10378506
Ng S, Valdes PA, Moritz-Gasser S, Lemaitre AL, Duffau H, Herbet G (2023) Intraoperative functional remapping unveils evolving patterns of cortical plasticity. Brain 146:3088–3100. https://doi.org/10.1093/brain/awad116
doi: 10.1093/brain/awad116
pubmed: 37029961
Obara T, Blonski M, Brzenczek C et al (2020) Adult diffuse low-Grade gliomas: 35-Year experience at the Nancy France Neurooncology Unit. Front Oncol 10:574679. https://doi.org/10.3389/fonc.2020.574679
doi: 10.3389/fonc.2020.574679
pubmed: 33194684
pmcid: 7656991
Picart T, Herbet G, Moritz-Gasser S, Duffau H (2019) Iterative Surgical resections of diffuse glioma with Awake Mapping: how to deal with cortical plasticity and connectomal constraints? Neurosurgery 85:105–116. https://doi.org/10.1093/neuros/nyy218
doi: 10.1093/neuros/nyy218
pubmed: 30010996
Ribeiro L, Ng S, Duffau H (2022) Recurrent insular low-grade gliomas: factors guiding the decision to reoperate. J Neurosurg 138:1216–1226. https://doi.org/10.3171/2022.9.JNS221286
doi: 10.3171/2022.9.JNS221286
pubmed: 36308479
Roelz R, Strohmaier D, Jabbarli R et al (2016) Residual tumor volume as best outcome predictor in low Grade Glioma - A Nine-Years Near-Randomized Survey of surgery vs. Biopsy Sci Rep 6:32286. https://doi.org/10.1038/srep32286
doi: 10.1038/srep32286
pubmed: 27574036
Rossi M, Gay L, Ambrogi F et al (2021) Association of supratotal resection with progression-free survival, malignant transformation, and overall survival in lower-grade gliomas. Neuro Oncol 23:812–826. https://doi.org/10.1093/neuonc/noaa225
doi: 10.1093/neuonc/noaa225
pubmed: 33049063
Sarubbo S, Tate M, De Benedictis A et al (2020) Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain. NeuroImage 205:116237. https://doi.org/10.1016/j.neuroimage.2019.116237
doi: 10.1016/j.neuroimage.2019.116237
pubmed: 31626897
Shofty B, Haim O, Costa M et al (2020) Impact of repeated operations for progressive low-grade gliomas. Eur J Surg Oncol 46:2331–2337. https://doi.org/10.1016/j.ejso.2020.07.013
doi: 10.1016/j.ejso.2020.07.013
pubmed: 32771251
Southwell DG, Hervey-Jumper SL, Perry DW, Berger MS (2016) Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex. J Neurosurg 124:1460–1469. https://doi.org/10.3171/2015.5.JNS142833
doi: 10.3171/2015.5.JNS142833
pubmed: 26544767
Zattra CM, Zhang DY, Broggi M et al (2019) Repeated craniotomies for intracranial tumors: is the risk increased? Pooled analysis of two prospective, institutional registries of complications and outcomes. J Neurooncol 142:49–57. https://doi.org/10.1007/s11060-018-03058-y
doi: 10.1007/s11060-018-03058-y
pubmed: 30474767
Zinsz A, Pouget C, Rech F et al (2024) The role of [18 F]FDOPA PET as an adjunct to conventional MRI in the diagnosis of aggressive glial lesions. Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-024-06720-y