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Oncological, cognitive, and employment outcomes in a series of patients with IDH-mutated glioma resected following neoadjuvant chemotherapy

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Abstract

Purpose

Maximal safe tumor resection is the first line of treatment for IDH-mutated gliomas. However, when upfront surgical resection is deemed unsatisfactory due to tumor size and location, chemotherapy could represent an interesting alternative for reducing glioma extension and allowing for a safer and more efficient removal.

Methods

We performed a retrospective study (June 2011 to December 2021) on patients with IDH-mutated gliomas undergoing chemotherapy with a neoadjuvant intent, followed by surgical excision in awake conditions. MRI-imaging follow-up was conducted every 3–6 months. Neuropsychological assessments (NPSA) were performed for all patients before surgery, during post-operative period, and at later follow-up, and patients were periodically interviewed about their clinical and job status.

Results

We included 6 patients who underwent awake surgery after neoadjuvant chemotherapy (temozolomide in 5 cases, PCV in 1 case) for an IDH-mutated glioma (3 oligodendrogliomas and 3 astrocytomas). Median tumor volume reduction was 47%, allowing for complete resection in one patient, subtotal resection in 4 patients, and partial resection in 1 patient. No major adverse effects were observed under chemotherapy. At the 4 months NPSA, a worsening of flexibility was observed in 2 patients (verbal fluencies in one case and trail making test in the other). Three out of the four patients working full time before procedure resumed their job full time, after a 7 to 10 months delay.

Conclusion

Neoadjuvant chemotherapy followed by maximal safe resection can be offered to patients affected by IDH-mutated gliomas for whom upfront surgery would be inadequate. More studies are necessary given the limited size of our sample.

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References

  1. Amelot A, De Cremoux P, Quillien V et al (2015) IDH-Mutation is a weak predictor of long-term survival in glioblastoma patients. PLoS One 10(7):e0130596

    Article  PubMed  PubMed Central  Google Scholar 

  2. Berger MS, Deliganis AV, Dobbins J, Keles GE (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74(6):1784–1791

    Article  CAS  PubMed  Google Scholar 

  3. Blonski M, Taillandier L, Herbet G et al (2012) Combination of neoadjuvant chemotherapy followed by surgical resection as a new strategy for WHO grade II gliomas: a study of cognitive status and quality of life. J Neuro-Oncol 106(2):353–366

    Article  CAS  Google Scholar 

  4. Blonski M, Pallud J, Gozé C et al (2013) Neoadjuvant chemotherapy may optimize the extent of resection of World Health Organization grade II gliomas: a case series of 17 patients. J Neuro-Oncol 113(2):267–275

    Article  CAS  Google Scholar 

  5. Cairncross G, Wang M, Shaw E et al (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 31(3):337–343

    Article  CAS  PubMed  Google Scholar 

  6. CogniSciences | Outils | ÉCLA-16+. http://www.cognisciences.com/accueil/outils/article/ecla-16. Accessed 16 Jun 2022

  7. de Leeuw CN, Vogelbaum MA (2019) Supratotal resection in glioma: a systematic review. Neuro-Oncol 21(2):179–188

    Article  PubMed  Google Scholar 

  8. Duffau H, Taillandier L, Capelle L (2006) Radical surgery after chemotherapy: a new therapeutic strategy to envision in grade II glioma. J Neuro-Oncol 80(2):171–176

    Article  Google Scholar 

  9. Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L (2008) Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109(3):461–471

    Article  PubMed  Google Scholar 

  10. Gauthier L, Dehaut F, Joanette Y (1989) The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 11(2):49–54

  11. Harrison JE, Buxton P, Husain M, Wise R (2000) Short test of semantic and phonological fluency: normal performance, validity and test-retest reliability. Br J Clin Psychol 39(2):181–191

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. Hilbert S, Nakagawa TT, Puci P, Zech A, Bühner M (2015) The digit span backwards task: verbal and visual cognitive strategies in working memory assessment. Eur J Psychol Assess 31(3):174–180

    Article  Google Scholar 

  14. Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgård G, Solheim O (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 308(18):1881–1888

    Article  CAS  PubMed  Google Scholar 

  15. Jo J, Williams B, Smolkin M, Wintermark M, Shaffrey ME, Lopes MB, Schiff D (2014) Effect of neoadjuvant temozolomide upon volume reduction and resection of diffuse low-grade glioma. J Neuro-Oncol 120(1):155–161

    Article  CAS  Google Scholar 

  16. Llinàs-Reglà J, Vilalta-Franch J, López-Pousa S, Calvó-Perxas L, Torrents Rodas D, Garre-Olmo J (2017) The trail making test. Assessment 24(2):183–196

    Article  PubMed  Google Scholar 

  17. 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(8):1231–1251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mandonnet E, Duffau H (2018) An attempt to conceptualize the individual onco-functional balance: Why a standardized treatment is an illusion for diffuse low-grade glioma patients. Crit Rev Oncol Hematol 122:83–91

    Article  PubMed  Google Scholar 

  19. Mandonnet E, Duffau H, Bauchet L (2012) A new tool for grade II glioma studies: plotting cumulative time with quality of life versus time to malignant transformation. J Neuro-Oncol 106(1):213–215

    Article  Google Scholar 

  20. Mandonnet E, Mellerio C, Barberis M, Poisson I, Jansma JM, Rutten G-J (2020) When right is on the left (and vice versa): a case series of glioma patients with reversed lateralization of cognitive functions. J Neurol Surg A Cent Eur Neurosurg 81(02):138–146

    Article  PubMed  Google Scholar 

  21. Metz-Lutz MN, Kremin H, Deloche G, et al Standardisation d’un test de dénomination orale: contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. 9

  22. Moritz-Gasser S, Duffau H (2013) The anatomo-functional connectivity of word repetition: insights provided by awake brain tumor surgery. Front Hum Neurosci 7:405

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gronwall DM (1977) Paced auditory serial-addition task: a measure of recovery from concussion. Percept Mot Skills 44(2):367–373

    Article  CAS  PubMed  Google Scholar 

  24. Pallud J, Rigaux-Viode O, Corns R, Muto J, Lopez Lopez C, Mellerio C, Sauvageon X, Dezamis E (2017) Direct electrical bipolar electrostimulation for functional cortical and subcortical cerebral mapping in awake craniotomy. Practical considerations. Neurochirurgie 63(3):164–174

    Article  CAS  PubMed  Google Scholar 

  25. Park J, Jeong E, Seomun G (2018) The clock drawing test: a systematic review and meta-analysis of diagnostic accuracy. J Adv Nurs 74(12):2742–2754

    Article  PubMed  Google Scholar 

  26. Pascual JSG, Duffau H (2022) The need to consider return to work as a main outcome in patients undergoing surgery for diffuse low-grade glioma: a systematic review. Acta Neurochir 164(10):2789–2809

    Article  PubMed  Google Scholar 

  27. Peyre M, Cartalat-Carel S, Meyronet D et al (2010) Prolonged response without prolonged chemotherapy: a lesson from PCV chemotherapy in low-grade gliomas. Neuro-Oncol 12(10):1078–1082

    Article  PubMed  PubMed Central  Google Scholar 

  28. Protocole Montréal d’Évaluation de la Communication (MEC). CRIUGM

  29. Ricard D, Kaloshi G, Amiel-Benouaich A et al (2007) Dynamic history of low-grade gliomas before and after temozolomide treatment. Ann Neurol 61(5):484–490

    Article  CAS  PubMed  Google Scholar 

  30. Roelz R, Strohmaier D, Jabbarli R, Kraeutle R, Egger K, Coenen VA, Weyerbrock A, Reinacher PC (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Scarpina F, Tagini S (2017) The stroop color and word test. Front Psychol 8:557

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sjöberg RL, Stålnacke M, Andersson M, Eriksson J (2019) The supplementary motor area syndrome and cognitive control. Neuropsychologia 129:141–145

    Article  PubMed  Google Scholar 

  33. Spena G, Garbossa D, Barletta L, Prevost C, Versari P (2010) Preoperative chemotherapy for infiltrative low-grade oligoastrocytoma: a useful strategy to maximize surgical resection -case report-: —case report—. Neurol Med Chir (Tokyo) 50(5):410–413

    Article  PubMed  Google Scholar 

  34. Steinborn MB, Langner R, Flehmig HC, Huestegge L (2018) Methodology of performance scoring in the d2 sustained-attention test: cumulative-reliability functions and practical guidelines. Psychol Assess 30(3):339–357

    Article  PubMed  Google Scholar 

  35. S S, S E, O’Hara D, Maguire M, E W, G B, C L, Chumas P, Goodden J (2015) Tailoring the extent of resection using specialist speech therapy assessment during awake craniotomy for Low Grade Glioma.

  36. Strauss E, Spreen O (1990) A comparison of the Rey and Taylor figures. Arch Clin Neuropsychol 5(4):417–420

    Article  CAS  PubMed  Google Scholar 

  37. The Pyramids and Palm Trees Test. https://www.pearsonassessments.com/store/usassessments/en/Store/Professional-Assessments/Cognition-%26-Neuro/The-Pyramids-and-Palm-Trees-Test/p/100000185.html. Accessed 16 Jun 2022

  38. Van der Linden M, Coyette F, Poitrenaud J (2004) L’épreuve de rappel libre/rappel indicé à 16 items (RL/RI-16). Lévaluation Troubl Mém:25–47

  39. Weller M, van den Bent M, Tonn JC et al (2017) European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol 18(6):e315–e329

    Article  PubMed  Google Scholar 

  40. 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

    Article  PubMed  Google Scholar 

  41. Weller J, Katzendobler S, Karschnia P, Lietke S, Egensperger R, Thon N, Weller M, Suchorska B, Tonn J-C (2021) PCV chemotherapy alone for WHO grade 2 oligodendroglioma: prolonged disease control with low risk of malignant progression. J Neuro-Oncol 153(2):283–291

    Article  CAS  Google Scholar 

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Acknowledgements

EM was supported by INSERM (Contrat Interface 2018).

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Correspondence to Emmanuel Mandonnet.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee of Lariboisière Hospital and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Oral consent to use clinical data for research purpose was collected in written by the clinicians.

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Bursi, M., Rizzo, C., Barberis, M. et al. Oncological, cognitive, and employment outcomes in a series of patients with IDH-mutated glioma resected following neoadjuvant chemotherapy. Acta Neurochir 165, 2461–2471 (2023). https://doi.org/10.1007/s00701-023-05711-6

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