Abstract
Background
National guidelines recommend maximal safe resection of low-grade and high-grade oligodendrogliomas. However, there is no level 1 evidence to support these guidelines, and recent retrospective studies on the topic have yielded mixed results.
Objective
To assess the association between extent of resection (EOR) and survival for oligodendrogliomas in the general U.S. population.
Methods
Cases diagnosed between 2004 and 2013 were selected from the Surveillance, Epidemiology, and End-Results (SEER) Program and retrospectively analyzed for treatment, prognostic factors, and survival times. Cases that did not undergo tumor de-bulking surgery (e.g. no surgery or biopsy alone) were compared to subtotal resection (resection) and gross-total resection (GTR). The primary end-points were overall survival (OS) and cause-specific survival (CSS). An external validation cohort with 1p/19q-codeleted tumors was creating using the TCGA and GSE16011 datasets.
Results
3135 Cases were included in the final analysis. The 75% survival time (75ST) and 5-year survival rates were 47 months and 70.8%, respectively. Subtotal resection (STR, 75ST = 50 months) and GTR (75ST = 61 months) were associated with improved survival times compared to cases that did not undergo surgical debulking (75ST = 20 months, P < 0.001 for both), with reduced hazard ratios (HRs) after controlling for other factors (HR 0.81 [0.68–0.97] and HR 0.65 [0.54–0.79], respectively). GTR was associated with improved OS in both low-grade and anaplastic oligodendroglioma subgroups (HR 0.74 [0.58–0.95], HR 0.60 [0.44–0.82], respectively) while STR fell short of significance in the subgroup analysis. All findings were corroborated by multivariable analysis of CSS and externally validated in a cohort of patients with 1p19q-codeleted tumors.
Conclusion
Greater EOR is associated with improved survival in oligodendrogliomas. Our findings in this U.S. population-based cohort support national guidelines.
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Abbreviations
- SEER:
-
Surveillance, Epidemiology, and End-Results
- OS:
-
Overall survival
- CSS:
-
Cause-specific survival
- STR:
-
Subtotal resection
- GTR:
-
Gross total resection
- HR:
-
Hazard ratio
- 75ST:
-
75% Survival time
- O2:
-
Grade II oligodendrogliomas
- O3:
-
Grade III oligodendrogliomas
- LGG:
-
Low-grade glioma
- HGG:
-
High-grade glioma
- NCCN:
-
National Comprehensive Cancer Network
- EOR:
-
Extent of resection
References
Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neurooncology 17(Suppl 4):iv1–iv62. https://doi.org/10.1093/neuonc/nov189
Keles GE, Lamborn KR, Berger MS (2001) Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. J Neurosurg 95:735–745. https://doi.org/10.3171/jns.2001.95.5.0735
Lindegaard KF, Mork SJ, Eide GE, Halvorsen TB, Hatlevoll R, Solgaard T, Dahl O, Ganz J (1987) Statistical analysis of clinicopathological features, radiotherapy, and survival in 170 cases of oligodendroglioma. J Neurosurg 67:224–230. https://doi.org/10.3171/jns.1987.67.2.0224
Berger MS, Rostomily RC (1997) Low grade gliomas: functional mapping resection strategies, extent of resection, and outcome. J Neurooncol 34:85–101
Stupp R, Brada M, van den Bent MJ, Tonn JC, Pentheroudakis G, ESMO Guidelines Working Group (2014) High-grade glioma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 25(Suppl 3):iii93–101. https://doi.org/10.1093/annonc/mdu050
National Comprehensive Cancer Network (2016) NCCN clinical practice guidelines in oncology: central nervous system cancers (version 1.2016). National Comprehensive Cancer Network. www.nccn.org. Accessed 14 May 2019
Grier JT, Batchelor T (2006) Low-grade gliomas in adults. Oncologist 11:681–693. https://doi.org/10.1634/theoncologist.11-6-681
Forst DA, Nahed BV, Loeffler JS, Batchelor TT (2014) Low-grade gliomas. Oncologist 19:403–413. https://doi.org/10.1634/theoncologist.2013-0345
Alattar AA, Brandel MG, Hirshman BR, Dong X, Carroll KT, Ali MA, Carter BS, Chen CC (2018) Oligodendroglioma resection: a Surveillance, Epidemiology, and End Results (SEER) analysis. J Neurosurg 128:1076–1083. https://doi.org/10.3171/2016.11.JNS161974
El-Hateer H, Souhami L, Roberge D, Maestro RD, Leblanc R, Eldebawy E, Muanza T, Melancon D, Kavan P, Guiot MC (2009) Low-grade oligodendroglioma: an indolent but incurable disease? Clinical article. J Neurosurg 111:265–271. https://doi.org/10.3171/2008.11.JNS08983
Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24:1236–1245. https://doi.org/10.1200/JCO.2005.05.2399
Lebrun C, Fontaine D, Ramaioli A, Vandenbos F, Chanalet S, Lonjon M, Michiels JF, Bourg V, Paquis P, Chatel M, Frenay M, Nice Brain Tumor Study Group (2004) Long-term outcome of oligodendrogliomas. Neurology 62:1783–1787
Lindegaard K-F, Mørk SJ, Eide GE, Halvorsen TB, Hatlevoll R, Solgaard T, Dahl O, Ganz J (1987) Statistical analysis of clinicopathological features, radiotherapy, and survival in 170 cases of oligodendroglioma. J Neurosurg 67:224–230. https://doi.org/10.3171/jns.1987.67.2.0224
Nagy M, Schulz-Ertner D, Bischof M, Welzel T, Hof H, Debus J, Combs SE (2009) Long-term outcome of postoperative irradiation in patients with newly diagnosed WHO grade III anaplastic gliomas. Tumori 95:317–324
Nuno M, Birch K, Mukherjee D, Sarmiento JM, Black KL, Patil CG (2013) Survival and prognostic factors of anaplastic gliomas. Neurosurgery 73:458–465. https://doi.org/10.1227/01.neu.0000431477.02408.5e
Piepmeier J, Baehring JM (2004) Surgical resection for patients with benign primary brain tumors and low grade gliomas. J Neurooncol 69:55–65
Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338–1345. https://doi.org/10.1200/JCO.2007.13.9337
Snyder LA, Wolf AB, Oppenlander ME, Bina R, Wilson JR, Ashby L, Brachman D, Coons SW, Spetzler RF, Sanai N (2014) The impact of extent of resection on malignant transformation of pure oligodendrogliomas. J Neurosurg 120:309–314. https://doi.org/10.3171/2013.10.JNS13368
Thon N, Kreth FW, Tonn JC (2015) The role of surgery in grade II/III oligodendroglial tumors. CNS Oncol 4:317–323. https://doi.org/10.2217/cns.15.26
Yang LS, Huang FP, Zheng K, Zhang HS, Zhou X, Bao XH, Zheng JJ, Chang C, Zhou LF (2010) Factors affecting prognosis of patients with intracranial anaplastic oligodendrogliomas: a single institutional review of 70 patients. J Neurooncol 100:113–120. https://doi.org/10.1007/s11060-010-0146-4
Jiang H, Zhang Z, Ren X, Zeng W, Jia W, Wang J, Lin S (2014) 1p/19q-driven prognostic molecular classification for high-grade oligodendroglial tumors. J Neurooncol 120:607–614. https://doi.org/10.1007/s11060-014-1593-0
Watanabe T, Nobusawa S, Kleihues P, Ohgaki H (2009) IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol 174:1149–1153. https://doi.org/10.2353/ajpath.2009.080958
Chamberlain MC, Born D (2015) Prognostic significance of relative 1p/19q codeletion in oligodendroglial tumors. J Neurooncol 125:249–251. https://doi.org/10.1007/s11060-015-1906-y
Overview of the SEER Program. National Cancer Institute Surveillance, Epidemiology, and End Results Program. https://seer.cancer.gov/about/overview.html. Accessed 19 Aug 2017
Davis FG, McCarthy BJ, Berger MS (1999) Centralized databases available for describing primary brain tumor incidence, survival, and treatment: Central Brain Tumor Registry of the United States; Surveillance, Epidemiology, and End Results; and National Cancer Data Base. Neurooncology 1:205–211. https://doi.org/10.1093/neuonc/1.3.205
Kinslow CJ, Bruce SS, Rae AI, Sheth SA, McKhann GM, Sisti MB, Bruce JN, Sonabend AM, Wang TJC (2018) Solitary-fibrous tumor/hemangiopericytoma of the central nervous system: a population-based study. J Neurooncol 138:173–182. https://doi.org/10.1007/s11060-018-2787-7
Rae AI, Mehta A, Cloney M, Kinslow CJ, Wang TJC, Bhagat G, Canoll PD, Zanazzi GJ, Sisti MB, Sheth SA, Connolly ES, McKhann GM, Bruce JN, Iwamoto FM, Sonabend AM (2018) Craniotomy and survival for primary central nervous system lymphoma. Neurosurgery. https://doi.org/10.1093/neuros/nyy096
Zhou Z, Kinslow CJ, Hibshoosh H, Guo H, Cheng SK, He C, Gentry MS, Sun RC (2019) Clinical features, survival and prognostic factors of glycogen-rich clear cell carcinoma (GRCC) of the breast in the U.S. population. J Clin Med. https://doi.org/10.3390/jcm8020246
The Cancer Genome Atlas Program (2019). National Cancer Institute. https://www.cancer.gov/about-nci/organization/ccg/research/structural-genomics/tcga. Accessed 10 May 2019
Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas (2015). N Engl J Med 372:2481–2498. https://doi.org/10.1056/NEJMoa1402121
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1
Gravendeel LAM, Kouwenhoven MCM, Gevaert O, de Rooi JJ, Stubbs AP, Duijm JE, Daemen A, Bleeker FE, Bralten LBC, Kloosterhof NK, De Moor B, Eilers PHC, van der Spek PJ, Kros JM, Sillevis Smitt PAE, van den Bent MJ, French PJ (2009) Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res 69:9065. https://doi.org/10.1158/0008-5472.CAN-09-2307
Surveillance, Epidemiology, and End Results (SEER) Program. SEER*Stat Database: Incidence—SEER 9 Regs Research Data, Nov 2015 Sub (1973–2013) %3cKatrina/Rita Population Adjustment%3e—Linked To County Attributes—Total U.S., 1969–2014 Counties. www.seer.cancer.gov (released April 2016, based on the November 2015 submission). Accessed 14 May 2019
Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neurooncology 17:iv1–iv62. https://doi.org/10.1093/neuonc/nov189
Facility Oncology Registry Data Standards, FORDS (2013): revised for 2013. American College of Surgeons. https://www.facs.org/~/media/files/quality%20programs/cancer/coc/fords/fords%20manual%202013.ashx
Schupper AJ, Hirshman BR, Carroll KT, Ali MA, Carter BS, Chen CC (2017) Effect of gross total resection in World Health Organization Grade II astrocytomas: SEER-based survival analysis. World Neurosurg 103:741–747. https://doi.org/10.1016/j.wneu.2017.03.140
Dong X, Noorbakhsh A, Hirshman BR, Zhou T, Tang JA, Chang DC, Carter BS, Chen CC (2016) Survival trends of grade I, II, and III astrocytoma patients and associated clinical practice patterns between 1999 and 2010: a SEER-based analysis. Neurooncol Pract 3:29–38. https://doi.org/10.1093/nop/npv016
Carroll KT, Hirshman B, Ali MA, Alattar AA, Brandel MG, Lochte B, Lanman T, Carter B, Chen CC (2017) Management and survival patterns of patients with gliomatosis cerebri: a SEER-based analysis. World Neurosurg 103:186–193. https://doi.org/10.1016/j.wneu.2017.03.103
Brandel MG, Alattar AA, Hirshman BR, Dong X, Carroll KT, Ali MA, Carter BS, Chen CC (2017) Survival trends of oligodendroglial tumor patients and associated clinical practice patterns: a SEER-based analysis. J Neurooncol. https://doi.org/10.1007/s11060-017-2430-z
Vasista A, Stockler MR, West T, Wilcken N, Kiely BE (2017) More than just the median: calculating survival times for patients with HER2 positive, metastatic breast cancer using data from recent randomised trials. Breast 31:99–104. https://doi.org/10.1016/j.breast.2016.10.007
Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, Berger MS, Parsa AT (2012) Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. J Neurosurg 117:1032–1038. https://doi.org/10.3171/2012.9.JNS12504
Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:3–8. https://doi.org/10.3171/2011.2.JNS10998
Lassman AB, Iwamoto FM, Cloughesy TF, Aldape KD, Rivera AL, Eichler AF, Louis DN, Paleologos NA, Fisher BJ, Ashby LS, Cairncross JG, Roldan GB, Wen PY, Ligon KL, Schiff D, Robins HI, Rocque BG, Chamberlain MC, Mason WP, Weaver SA, Green RM, Kamar FG, Abrey LE, DeAngelis LM, Jhanwar SC, Rosenblum MK, Panageas KS (2011) International retrospective study of over 1000 adults with anaplastic oligodendroglial tumors. Neurooncology 13:649–659. https://doi.org/10.1093/neuonc/nor040
Jeremic B, Shibamoto Y, Gruijicic D, Milicic B, Stojanovic M, Nikolic N, Dagovic A, Aleksandrovic J (1999) Combined treatment modality for anaplastic oligodendroglioma: a phase II study. J Neurooncol 43:179–185
van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Haaxma-Reiche H, Kros JM, van Kouwenhoven MC, Vecht CJ, Allgeier A, Lacombe D, Gorlia T (2006) Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol 24:2715–2722. https://doi.org/10.1200/JCO.2005.04.6078
Intergroup Radiation Therapy Oncology Group Trial, Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, Brachman D, Buckner J, Fink K, Souhami L, Laperierre N, Mehta M, Curran W (2006) Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol 24:2707–2714. https://doi.org/10.1200/JCO.2005.04.3414
Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:997–1003. https://doi.org/10.1016/S1470-2045(11)70196-6
Darefsky AS, King JT, Dubrow R (2011) Adult glioblastoma multiforme survival in the temozolomide era: a population-based analysis of Surveillance, Epidemiology, and End Results registries. Cancer 118:2163–2172. https://doi.org/10.1002/cncr.26494
Aghi MK, Nahed BV, Sloan AE, Ryken TC, Kalkanis SN, Olson JJ (2015) The role of surgery in the management of patients with diffuse low grade glioma: a systematic review and evidence-based clinical practice guideline. J Neurooncol 125:503–530. https://doi.org/10.1007/s11060-015-1867-1
Bonney PA, Boettcher LB, Burks JD, Baker C, Conner AK, Fujii T, Mehta VA, Briggs RG, Sughrue ME (2017) Rates of seizure freedom after surgical resection of diffuse low-grade gliomas. World Neurosurg 106:750–756. https://doi.org/10.1016/j.wneu.2017.06.144
Kahn J, Loeffler JS, Niemierko A, Chiocca EA, Batchelor T, Chakravarti A (2011) Long-term outcomes of patients with spinal cord gliomas treated by modern conformal radiation techniques. Int J Radiat Oncol Biol Phys 81:232–238. https://doi.org/10.1016/j.ijrobp.2010.05.009
Karhade AV, Larsen AMG, Cote DJ, Dubois HM, Smith TR (2018) National databases for neurosurgical outcomes research: options, strengths, and limitations. Neurosurgery 83:333–344. https://doi.org/10.1093/neuros/nyx408
Buckner JC, Shaw EG, Pugh SL, Chakravarti A, Gilbert MR, Barger GR, Coons S, Ricci P, Bullard D, Brown PD, Stelzer K, Brachman D, Suh JH, Schultz CJ, Bahary JP, Fisher BJ, Kim H, Murtha AD, Bell EH, Won M, Mehta MP, Curran WJ Jr (2016) Radiation plus procarbazine, CCNU, and vincristine in low-grade glioma. N Engl J Med 374:1344–1355. https://doi.org/10.1056/NEJMoa1500925
Wesseling P, van den Bent M, Perry A (2015) Oligodendroglioma: pathology, molecular mechanisms and markers. Acta Neuropathol 129:809–827. https://doi.org/10.1007/s00401-015-1424-1
Alluri RK, Leland H, Heckmann N (2016) Surgical research using national databases. Ann Transl Med 4:393. https://doi.org/10.21037/atm.2016.10.49
Cooper GS, Virnig B, Klabunde CN, Schussler N, Freeman J, Warren JL (2002) Use of SEER-Medicare data for measuring cancer surgery. Med Care 40:IV-43–IV-48
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 2:1460–1469. https://doi.org/10.1001/jamaoncol.2016.1373
Aizer AA, Bi WL, Kandola MS, Lee EQ, Nayak L, Rinne ML, Norden AD, Beroukhim R, Reardon DA, Wen PY, Al-Mefty O, Arvold ND, Dunn IF, Alexander BM (2015) Extent of resection and overall survival for patients with atypical and malignant meningioma. Cancer 121:4376–4381. https://doi.org/10.1002/cncr.29639
Warren JL, Harlan LC (2003) Can cancer registry data be used to study cancer treatment? Med Care 41:1003–1005. https://doi.org/10.1097/01.MLR.0000086827.00805.B5
Kinslow CJ, Rajpara RS, Wu C-C, Bruce SS, Canoll PD, Wang S-H, Sonabend AM, Sheth SA, McKhann GM, Sisti MB, Bruce JN, Wang TJC (2017) Invasiveness is associated with metastasis and decreased survival in hemangiopericytoma of the central nervous system. J Neurooncol. https://doi.org/10.1007/s11060-017-2450-8
Kinslow CJ NA, Adams CM, Sheth SA, McKhann GM, Sisti MB, Bruce JN, Iwamoto FM, Sonabend AM, Wang TJ. Surgery plus adjuvant radiation for primary central nervous system lymphoma. J Neurosurg
Merrill RM, Capocaccia R, Feuer EJ, Mariotto A (2000) Cancer prevalence estimates based on tumour registry data in the Surveillance, Epidemiology, and End Results (SEER) Program. Int J Epidemiol 29:197–207
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No outside funding was received to support this work. Dr. Wang reports personal fees and non-financial support from AbbVie, personal fees and non-financial support from Merck, personal fees from AstraZeneca, personal fees from Doximity, personal fees and non-financial support from Novocure, personal fees and non-financial support from Elekta, personal fees from Cancer Panels, personal fees and non-financial support from RTOG Foundation, and personal fees from Wolters Kluwer, outside the submitted work. Dr. Neugut has served as a Consultant to Pfizer, Teva, Otsuka, Eisai, and United Biosource Corporation and is on the Medical Advisory Board of EHE, Intl.
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Kinslow, C.J., Garton, A.L., Rae, A.I. et al. Extent of resection and survival for oligodendroglioma: a U.S. population-based study. J Neurooncol 144, 591–601 (2019). https://doi.org/10.1007/s11060-019-03261-5
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DOI: https://doi.org/10.1007/s11060-019-03261-5