Abstract
Purpose
Aggressive resection in surgically-accessible glioblastoma (GBM) correlates with improved survival over less extensive resections. However, the clinical impact of performing a biopsy before definitive resection have not been previously evaluated.
Methods
We analyzed 17,334 GBM patients from the NCDB from 2010–2014. We categorized them into: “upfront resection” and “biopsy followed by resection”. The outcomes of interes included OS, 30-day readmission/mortality, 90-day mortality, and length of hospital stay (LOS). The Kaplan–Meier methods and accelerated failure time (AFT) models were applied for survival analysis. Multivariable binary logistic regression were performed to compare differences among groups. Multiple imputation and propensity score matching (PSM) were conducted for validation.
Results
“Upfront resection” had superior OS over “biopsy followed by resection” (median OS:12.4 versus 11.1 months, log-rank p = 0.001). Similarly, multivariable AFT models favored “upfront resection" (time ratio[TR]:0.83, 95%CI: 0.75–0.93, p = 0.001). Patients undergoing “upfront gross-total resection (GTR)” had higher OS over “upfront subtotal resection (STR)”, “GTR following STR”, and “GTR or STR following initial biopsy” (14.4 vs. 10.3, 13.5, 13.3, and 9.1 months;TR: 1.00 [Ref.], 0.75, 0.82, 0.88, and 0.67). Recent years of diagnosis, higher income, facilities located in Southern regions, and treatment at academic facilities were significantly associated with the higher likelihood of undergoing upfront resection. Multivariable regression showed a decreased 30 and 90-day mortality for patients undergoing “upfront resection”, 73% and 44%, respectively (p < 0.001).
Conclusions
Pre-operative biopsies for surgically accessible GBM are associated with worse survival despite subsequent resection compared to patients undergoing upfront resection.
Similar content being viewed by others
Data availability
The National Cancer Database would be available for data application from https://www.facs.org/quality-programs/cancer-programs/national-cancer-database/.
Code availability
Not applicable.
References
Ostrom QT, Price M, Neff C et al (2023) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2016–2020. Neuro Oncol 25(Supplement_4):iv1–iv99
Korja M, Raj R, Seppa K, Luostarinen T, Malila N, Seppala M, Maenpaa H, Pitkaniemi J (2018) Glioblastoma survival is improving despite increasing incidence rates: A nationwide study between 2000 and 2013 in Finland. Available at SSRN: https://doi.org/10.2139/ssrn.3207930
Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996
Lakomy R, Kazda T, Selingerova I et al (2020) Real-world evidence in glioblastoma: stupp’s regimen after a decade. Front Oncol 10:840
Brown TJ, Brennan MC, Li M et al (2016) Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol 2(11):1460–1469
Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN (2017) Prognostic implications of extent of resection in glioblastoma: analysis from a large database. World Neurosurg 103:330–340
Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115(1):3–8
Chaichana KL, Jusue-Torres I, Navarro-Ramirez R et al (2014) Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16(1):113–122
National Cancer Database. ACS. https://www.facs.org/quality-programs/cancer-programs/national-cancer-database/. Accessed 13 Feb 2023
World Health Organization WHO (2013) International classification of diseases for oncology (ICD-O), 3rd edn., 1st revision. Geneva, Switzerland. https://apps.who.int/iris/handle/10665/96612. Accessed Feb 2024
Zhu P, Du XL, Zhu JJ, Esquenazi Y (2019) Improved survival of glioblastoma patients treated at academic and high-volume facilities: a hospital-based study from the National Cancer Database. J Neurosurg 132(2):491–502
Zhu P, Du X, Blanco A et al (2020) Epid-34. The detrimental effect of biopsy preceding resection in surgically accessible glioblastomas: results from the National Cancer Database. Neuro Oncol 22(Supplement_2):ii85–ii86
Zhu P, Du XL, Blanco AI et al (2019) Impact of facility type and volume in low-grade glioma outcomes. J Neurosurg 1–11. https://doi.org/10.3171/2019.6.JNS19409
Krex D, Klink B, Hartmann C et al (2007) Long-term survival with glioblastoma multiforme. Brain 130(Pt 10):2596–2606
Sonoda Y, Kumabe T, Watanabe M et al (2009) Long-term survivors of glioblastoma: clinical features and molecular analysis. Acta Neurochir (Wien) 151(11):1349–1358
Han Q, Liang H, Cheng P, Yang H, Zhao P (2020) Gross total vs. subtotal resection on survival outcomes in elderly patients with high-grade glioma: a systematic review and meta-analysis. Front Oncol 10:151
Karschnia P, Young JS, Dono A et al (2023) Prognostic validation of a new classification system for extent of resection in glioblastoma: a report of the RANO resect group. Neuro Oncol 25(5):940–954. https://doi.org/10.1093/neuonc/noac193
Molinaro AM, Hervey-Jumper S, Morshed RA et al (2020) Association of maximal extent of resection of contrast-enhanced and non–contrast-enhanced tumor with survival within molecular subgroups of patients with newly diagnosed glioblastoma. JAMA Oncol 6(4):495. https://doi.org/10.1001/jamaoncol.2019.6143
Lopez-Rivera V, Dono A, Lewis CT et al (2021) Extent of resection and survival outcomes of geriatric patients with glioblastoma: is there benefit from aggressive surgery? Clin Neurol Neurosurg 202:106474
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
Barker FG 2nd, Chang SM, Gutin PH et al (1998) Survival and functional status after resection of recurrent glioblastoma multiforme. Neurosurgery 42(4):709–720 (discussion 720-3)
Ringel F, Pape H, Sabel M et al (2016) Clinical benefit from resection of recurrent glioblastomas: results of a multicenter study including 503 patients with recurrent glioblastomas undergoing surgical resection. Neuro Oncol 18(1):96–104
van Linde ME, Brahm CG, de Witt Hamer PC et al (2017) Treatment outcome of patients with recurrent glioblastoma multiforme: a retrospective multicenter analysis. J Neurooncol 135(1):183–192
Goldman DA, Hovinga K, Reiner AS, Esquenazi Y, Tabar V, Panageas KS (2018) The relationship between repeat resection and overall survival in patients with glioblastoma: a time-dependent analysis. J Neurosurg 129(5):1231–1239
D’Amico RS, Cloney MB, Sonabend AM et al (2015) The safety of surgery in elderly patients with primary and recurrent glioblastoma. World Neurosurg 84(4):913–919
Morshed RA, Young JS, Gogos AJ et al (2022) Reducing complication rates for repeat craniotomies in glioma patients: a single-surgeon experience and comparison with the literature. Acta Neurochir 164(2):405–417
Lu VM, Goyal A, Graffeo CS et al (2019) Survival benefit of maximal resection for glioblastoma reoperation in the temozolomide era: a meta-analysis. World Neurosurg 127:31–37
Lu VM, Jue TR, McDonald KL, Rovin RA (2018) The survival effect of repeat surgery at glioblastoma recurrence and its trend: a systematic review and meta-analysis. World Neurosurg 115:453-459.e3
Baron RB, Kessler RA, Hadjipanayis CG (2019) Initial biopsy and early re-resection practices in the treatment of glioblastoma among AANS/CNS tumor section surgeons. J Neurooncol 144(3):529–534
Kim AA, Dono A, Khalafallah AM et al (2022) Early repeat resection for residual glioblastoma: decision-making among an international cohort of neurosurgeons. J Neurosurg 137(6):1618–1627
Chaichana KL, Garzon-Muvdi T, Parker S et al (2011) Supratentorial glioblastoma multiforme: the role of surgical resection versus biopsy among older patients. Ann Surg Oncol 18(1):239–245
Noorbakhsh A, Tang JA, Marcus LP et al (2014) Gross-total resection outcomes in an elderly population with glioblastoma: a SEER-based analysis. J Neurosurg 120(1):31–39
Goel NJ, Bird CE, Hicks WH, Abdullah KG (2021) Economic implications of the modern treatment paradigm of glioblastoma: an analysis of global cost estimates and their utility for cost assessment. J Med Econ 24(1):1018–1024
Xiao N, Zhu D, Xiao S (2018) Effects of continued psychological care toward brain tumor patients and their family members’ negative emotions. J Cancer Res Ther 14(Supplement):S202–S207
Starowicz-Filip A, Prochwicz K, Myszka A et al (2022) Subjective experience, cognitive functioning and trauma level of patients undergoing awake craniotomy due to brain tumor - preliminary study. Appl Neuropsychol Adult 29(5):983–992
Kalpathy-Cramer J, Gerstner ER, Emblem KE, Andronesi O, Rosen B (2014) Advanced magnetic resonance imaging of the physical processes in human glioblastoma. Cancer Res 74(17):4622–4637
Lawrence YR, Mishra MV, Werner-Wasik M et al (2012) Improving prognosis of glioblastoma in the 21st century: who has benefited most? Cancer 118(17):4228–4234
Hong MAC, Omar AT, Khu KJO (2022) Socioeconomic factors affecting survivorship of glioblastoma patients in the Philippines. J Clin Neurosci 98:89–95
Pollom EL, Fujimoto DK, Han SS, Harris JP, Tharin SA, Soltys SG (2018) Newly diagnosed glioblastoma: adverse socioeconomic factors correlate with delay in radiotherapy initiation and worse overall survival. J Radiat Res 59(suppl_1):i11–i18
Overcast WB, Davis KM, Ho CY et al (2021) Advanced imaging techniques for neuro-oncologic tumor diagnosis, with an emphasis on PET-MRI imaging of malignant brain tumors. Curr Oncol Rep 23(3):34
Shukla G, Alexander GS, Bakas S et al (2017) Advanced magnetic resonance imaging in glioblastoma: a review. Chin Clin Oncol 6(4):40
Eibl RH, Schneemann M (2023) Liquid biopsy and glioblastoma. Explor Target Antitumor Ther 4(1):28–41
Ronvaux L, Riva M, Coosemans A et al (2022) Liquid biopsy in glioblastoma. Cancers 14(14). https://doi.org/10.3390/cancers14143394
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
Zou P, Xu H, Chen P et al (2013) IDH1/IDH2 mutations define the prognosis and molecular profiles of patients with gliomas: a meta-analysis. PLoS ONE 8(7):e68782
Acknowledgements
Partial results of the present study were presented at the 25th annual meeting of the Society for Neuro-Oncology (SNO), in November 2020, in Austin, Texas.
Funding
None.
Author information
Authors and Affiliations
Contributions
Study design: Data collection: Data analysis: Manuscript draft writing: Manuscript editing: Manuscript approval: all authors.
Corresponding author
Ethics declarations
Ethics declaration
This study was exempted from the institutional ethics review board.
Consent to participate and publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhu, P., Pichardo-Rojas, P.S., Dono, A. et al. The detrimental effect of biopsy preceding resection in surgically accessible glioblastoma: results from the national cancer database. J Neurooncol (2024). https://doi.org/10.1007/s11060-024-04644-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11060-024-04644-z