The impact of surgery on the survival of patients with recurrent glioblastoma

Oumar Sacko; Alexandra Benouaich-Amiel; Pierre Brandicourt; Mahamadou Niaré; Saloua Charni; Clarissa Cavandoli; David Brauge; Isabelle Catalaa; Adam Brenner; Elizabeth Moyal; Franck-Emmanuel Roux

doi:10.4103/ajns.AJNS_180_20

Asian Journal of Neurosurgery, Table of Contents

CC BY-NC-ND 4.0 · Asian J Neurosurg 2021; 16(01): 1-7
DOI: 10.4103/ajns.AJNS_180_20

Research Article

The impact of surgery on the survival of patients with recurrent glioblastoma

Authors

Oumar Sacko^*

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
Alexandra Benouaich-Amiel^*

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
Pierre Brandicourt

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
Mahamadou Niaré

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France

³CNRS (Centre Recherche et Cognition), Toulouse
Saloua Charni

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France

³CNRS (Centre Recherche et Cognition), Toulouse
Clarissa Cavandoli

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
David Brauge

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
Isabelle Catalaa

⁴Neuroradiologie, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France
Adam Brenner

⁵Western University of Health Sciences, Pomona
Elizabeth Moyal

²Université Paul-Sabatier, Toulouse, France

⁶Harrison Medical Center, Bremerton, WA, USA
Franck-Emmanuel Roux

¹Pôle Neurosciences, Neurochirurgie, PPR, Centre Hospitalo-Universitaire de Toulouse

²Université Paul-Sabatier, Toulouse, France

³CNRS (Centre Recherche et Cognition), Toulouse

Abstract

Objective: The purpose of this study was to investigate the possible benefit of repeat surgery on overall survival for patients with recurrent glioblastoma multiforme (GBM). Methods: We performed a retrospective analysis of data from patients who presented with recurrent GBM over a 5-year period (n = 157), comparing baseline characteristics and survival for patients who had at least 1 new tumor resection followed by chemotherapy (reoperation group, n = 59) and those who received medical treatment only (no-reoperation group, n = 98) for recurrence. Results: The baseline characteristics of the two groups differed in terms of WHO performance status (better in the reoperation group), mean age (60 years in the reoperation group vs. 65 years in the no-reoperation group), mean interval to recurrence (3 months later in the reoperation group than in the no-reoperation group) and more gross total resections in the reoperation group. Nevertheless, the patients in the reoperation group had a higher rate [32.8%] of sensorimotor deficits than those of the no-reoperation group [14.2]. There was no significant difference in sex; tumor localization, side, or extent; MGMT status; MIB-1 labeling index; or Karnofsky Performance Status [KPS] score. After adjustment for age, the WHO performance status, interval of recurrence, and extent of resection at the first operation, multivariate analysis showed that median survival was significantly better in the reoperation group than in the no-reoperation group (22.9 vs. 14.61 months, P < 0.05). After a total of 69 repeat operations in 59 patients (10 had 2 repeat surgeries), we noted 13 temporary and 20 permanent adverse postoperative events, yielding a permanent complication rate of 28.99% (20/69). There was also a statistically significant (P = 0.029, Student's t-test) decrease in the mean KPS score after reoperation (mean preoperative KPS score of 89.34 vs. mean postoperative score of 84.91). Conclusion: Our retrospective study suggests that repeat surgery may be beneficial for patients with GBM recurrence who have good functional status (WHO performance status 0 and 1), although the potential benefits must be weighed against the risk of permanent complications, which occurred in almost 30% of the patients who underwent repeat resection in this series.

Key-words:

Extent of resection - glioblastoma - neuro-oncology - recurrence - redo surgery - reoperation

Full Text

References

References
1 Rigau V, Zouaoui S, Mathieu-Daudé H, Darlix A, Maran A, Trétarre B, et al. French brain tumor database: 5-year histological results on 25 756 cases. Brain Pathol 2011;21:633-44.
2 Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, et al. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro Oncol 2015;17 Suppl 4:iv1-62.
3 Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
4 Mariniello G, Peca C, De Caro Mdel B, Giamundo A, Donzelli R, Maiuri F. Glioblastoma in the elderly: The impact of advanced age on treatment and survival. J Neurol Surg A Cent Eur Neurosurg 2014;75:276-81.
5 Chaudhry NS, Shah AH, Ferraro N, Snelling BM, Bregy A, Madhavan K, et al. Predictors of long-term survival in patients with glioblastoma multiforme: Advancements from the last quarter century. Cancer Invest 2013;31:287-308.
6 Valduvieco I, Verger E, Bruna J, Caral L, Pujol T, Ribalta T, et al. Impact of radiotherapy delay on survival in glioblastoma. Clin Transl Oncol 2013;15:278-82.
7 Sun MZ, Oh T, Ivan ME, Clark AJ, Safaee M, Sayegh ET, et al. Survival impact of time to initiation of chemoradiotherapy after resection of newly diagnosed glioblastoma. J Neurosurg 2015;122:1144-50.
8 Chaichana KL, Zadnik P, Weingart JD, Olivi A, Gallia GL, Blakeley J, et al. Multiple resections for patients with glioblastoma: Prolonging survival. J Neurosurg 2013;118:812-20.
9 Stummer W, van den Bent MJ, Westphal M. Cytoreductive surgery of glioblastoma as the key to successful adjuvant therapies: New arguments in an old discussion. Acta Neurochir (Wien) 2011;153:1211-8.
10 Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, et al. Association of the extent of resection with survival in glioblastoma: A systematic review and meta-analysis. JAMA Oncol 2016;2:1460-9.
11 Hou LC, Veeravagu A, Hsu AR, Tse VC. Recurrent glioblastoma multiforme: A review of natural history and management options. Neurosurg Focus 2006;20:E5.
12 Nieder C, Grosu AL, Molls M. A comparison of treatment results for recurrent malignant gliomas. Cancer Treat Rev 2000;26:397-409.
13 Bauchet L, Mathieu-Daudé H, Fabbro-Peray P, Rigau V, Fabbro M, Chinot O, et al. Oncological patterns of care and outcome for 952 patients with newly diagnosed glioblastoma in 2004. Neuro Oncol 2010;12:725-35.
14 Ening G, Osterheld F, Capper D, Schmieder K, Brenke C. Risk factors for glioblastoma therapy associated complications. Clin Neurol Neurosurg 2015;134:55-9.
15 Oppenlander ME, Wolf AB, Snyder LA, Bina R, Wilson JR, Coons SW, et al. An extent of resection threshold for recurrent glioblastoma and its risk for neurological morbidity. J Neurosurg 2014;120:846-53.
16 Fischer CM, Neidert MC, Péus D, Ulrich NH, Regli L, Krayenbühl N, et al. Hydrocephalus after resection and adjuvant radiochemotherapy in patients with glioblastoma. Clin Neurol Neurosurg 2014;120:27-31.
17 Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: Response assessment in neuro-oncology working group. J Clin Oncol 2010;28:1963-72.
18 Burger PC, Dubois PJ, Schold SC Jr, Smith KR Jr, Odom GL, Crafts DC, et al. Computerized tomographic and pathologic studies of the untreated, quiescent, and recurrent glioblastoma multiforme. J Neurosurg 1983;58:159-69.
19 De Bonis P, Fiorentino A, Anile C, Balducci M, Pompucci A, Chiesa S, et al. The impact of repeated surgery and adjuvant therapy on survival for patients with recurrent glioblastoma. Clin Neurol Neurosurg 2013;115:883-6.
20 Lemée JM, Clavreul A, Aubry M, Com E, de Tayrac M, Eliat PA, et al. Characterizing the peritumoral brain zone in glioblastoma: A multidisciplinary analysis. J Neurooncol 2015;122:53-61.
21 Li R, Chen X, You Y, Wang X, Liu Y, Hu Q, et al. Comprehensive portrait of recurrent glioblastoma multiforme in molecular and clinical characteristics. Oncotarget 2015;6:30968-74.
22 Kim H, Zheng S, Amini SS, Virk SM, Mikkelsen T, Brat DJ, et al. Whole-genome and multisector exome sequencing of primary and post-treatment glioblastoma reveals patterns of tumor evolution. Genome Res 2015;25:316-27.
23 Christmann M, Nagel G, Horn S, Krahn U, Wiewrodt D, Sommer C, et al. MGMT activity, promoter methylation and immunohistochemistry of pretreatment and recurrent malignant gliomas: A comparative study on astrocytoma and glioblastoma. Int J Cancer 2010;127:2106-18.
24 Lonjon N, Bauchet L, Duffau H, Fabbro-Peray P, Segnarbieux F, Paquis P, et al. Second surgery for glioblastoma. A 4-year retrospective study conducted in both the Montpellier and Nice Departments of Neurosurgery. A literature review. Neurochirurgie 2010;56:36-42.
25 Menei P, Metellus P. Surgical treatment of glioblastomas. Neurochirurgie 2010;56:477-82.
26 Stark AM, Nabavi A, Mehdorn HM, Blömer U. Glioblastoma multiforme-report of 267 cases treated at a single institution. Surg Neurol 2005;63:162-9.
27 Barker FG 2nd, Chang SM, Gutin PH, Malec MK, McDermott MW, Prados MD, et al. Survival and functional status after resection of recurrent glioblastoma multiforme. Neurosurgery 1998;42:709-20.
28 Helseth R, Helseth E, Johannesen TB, Langberg CW, Lote K, Rønning P, et al. Overall survival, prognostic factors, and repeated surgery in a consecutive series of 516 patients with glioblastoma multiforme. Acta Neurol Scand 2010;122:159-67.
29 Mandl ES, Dirven CM, Buis DR, Postma TJ, Vandertop WP. Repeated surgery for glioblastoma multiforme: Only in combination with other salvage therapy. Surg Neurol 2008;69:506-9.
30 Barbagallo GM, Jenkinson MD, Brodbelt AR. 'Recurrent' glioblastoma multiforme, when should we reoperate? Br J Neurosurg 2008;22:452-5.
31 Robin AM, Lee I, Kalkanis SN. Reoperation for recurrent glioblastoma multiforme. Neurosurg Clin N Am 2017;28:407-28.
32 Gulati S, Jakola AS, Nerland US, Weber C, Solheim O. The risk of getting worse: Surgically acquired deficits, perioperative complications, and functional outcomes after primary resection of glioblastoma. World Neurosurg 2011;76:572-9.
33 Yoshikawa K, Kajiwara K, Morioka J, Fujii M, Tanaka N, Fujisawa H, et al. Improvement of functional outcome after radical surgery in glioblastoma patients: The efficacy of a navigation-guided fence-post procedure and neurophysiological monitoring. J Neurooncol 2006;78:91-7.
34 Woernle CM, Péus D, Hofer S, Rushing EJ, Held U, Bozinov O, et al. Efficacy of surgery and further treatment of progressive glioblastoma. World Neurosurg 2015;84:301-7.
35 Ening G, Huynh MT, Schmieder K, Brenke C. Repeat-surgery at Glioblastoma recurrence, when and why to operate? Clin Neurol Neurosurg 2015;136:89-94.
36 Terasaki M, Ogo E, Fukushima S, Sakata K, Miyagi N, Abe T, et al. Impact of combination therapy with repeat surgery and temozolomide for recurrent or progressive glioblastoma multiforme: A prospective trial. Surg Neurol 2007;68:250-4.
37 Hau P, Baumgart U, Pfeifer K, Bock A, Jauch T, Dietrich J, et al. Salvage therapy in patients with glioblastoma: Is there any benefit? Cancer 2003;98:2678-86.
38 Azizi A, Black P, Miyamoto C, Croul SE. Treatment of malignant astrocytomas with repetitive resections: A longitudinal study. Isr Med Assoc J 2001;3:254-7.
39 Wong ET, Hess KR, Gleason MJ, Jaeckle KA, Kyritsis AP, Prados MD, et al. Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J Clin Oncol 1999;17:2572-8.
40 Franceschi E, Bartolotti M, Tosoni A, Bartolini S, Sturiale C, Fioravanti A, et al. The effect of re-operation on survival in patients with recurrent glioblastoma. Anticancer Res 2015;35:1743-8.