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Journal of Neuro-Oncology

, Volume 140, Issue 3, pp 591–603 | Cite as

The prognostic value of maximal surgical resection is attenuated in oligodendroglioma subgroups of adult diffuse glioma: a multicenter retrospective study

  • Xiaojie Ding
  • Zheng Wang
  • Di Chen
  • Yinyan Wang
  • Zheng Zhao
  • Chongran Sun
  • Dikang Chen
  • Chao Tang
  • Ji Xiong
  • Lingchao Chen
  • Zhenwei Yao
  • Ying Liu
  • Xiaoqin Wang
  • Daniel P. Cahill
  • John F. de Groot
  • Tao Jiang
  • Yu Yao
  • Liangfu Zhou
Clinical Study

Abstract

Purpose

Maximal surgical resection is associated with survival benefit in the majority of studies in adult diffuse glioma. This study aims to characterize the prognostic value of surgical resection in molecular subgroups of diffuse glioma.

Methods

1178 patients with diffuse glioma from our centers and 422 from TCGA dataset were collected. The Kaplan–Meier analysis and multivariable Cox regression models were conducted to identify the prognostic value of surgical resection through different histological and molecular stratifications.

Results

Firstly, we confirmed progression-free survival (PFS) benefit associated with gross total resection (GTR) over sub-total resection (STR) in lower-grade glioma (HR 1.49; 95% CI 1.17–1.90; P = 0.001). Intriguingly however, we were unable to detect a significant PFS or overall survival (OS) benefit in oligodendroglioma (N = 397; HR 1.36; 95% CI 0.86–2.14; P = 0.19 and HR 1.05; 95% CI 0.55–1.99; P = 0.89, respectively). Secondly, when analyzed in molecular subgroups, we were similarly unable to detect a significant PFS or OS benefit in IDH MT/codel subgroup (N = 269; HR 1.47; 95% CI 0.92–2.34; P = 0.11 and HR 1.54; 95% CI 0.78–3.05; P = 0.21, respectively), oligodendroglioma with IDH MT/codel subgroup (N = 233; HR 1.33; 95% CI 0.79–2.21; P = 0.28 and HR 1.16; 95% CI 0.53–2.54; P = 0.70, respectively) or other relevant subgroups. TCGA validation also showed a significant survival benefit in astrocytoma rather than oligodendroglioma. Exploratory RNAseq analysis displayed that fewer cell proliferation-related gene expression features were specific to oligodendroglioma.

Conclusion

These results suggest that the benefit of maximal surgery may be attenuated in patients within oligodendroglioma relevant subgroups because of the chemosensitive and indolent nature. The aggressive surgery accompanying with risk of neurologic morbidity may be unnecessary for these patients given the lack of survival benefit with gross total resection.

Keywords

Glioma Extent of resection Prognostic value Molecular subgroup 

Notes

Acknowledgements

This study is supported by the Research Special Fund for Public Welfare Industry of Health (No. 201402008) to Yu Yao; the National Key Research and Development Plan (No. 2016YFC0902500) to Tao Jiang.

Author contributions

XD, TJ and YY designed the study. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, YL, XW, JFG, TJ and YY collected data. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, ZY, YL, JFG, TJ, YY and LZ provided materials. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, YL, XW, JFG, TJ and YY analyzed and interpreted the data. XD, ZW, DC, ZZ and XW did the statistical analyses. XD, ZW, DC, ZY, DPC, JFG, TJ, YY and LZ wrote and revised the manuscript. All authors approved the final report.

Compliance with ethical standards

Conflict of interest

We declare that we have no conflict of interest.

Supplementary material

11060_2018_2985_MOESM1_ESM.pdf (2.4 mb)
Supplementary material 1 (PDF 2451 KB)
11060_2018_2985_MOESM2_ESM.pdf (1.4 mb)
Supplementary material 2 (PDF 1412 KB)

References

  1. 1.
    Hervey-Jumper SL, Berger MS (2016) Maximizing safe resection of low- and high-grade glioma. J Neuro-oncol.  https://doi.org/10.1007/s11060-016-2110-4 Google Scholar
  2. 2.
    Albright AL, Wisoff JH, Zeltzer PM, Boyett JM, Rorke LB, Stanley P (1996) Effects of medulloblastoma resections on outcome in children: a report from the children’s cancer group. Neurosurgery 38:265–271CrossRefGoogle Scholar
  3. 3.
    DeAngelis LM, Seiferheld W, Schold SC, Fisher B, Schultz CJ, Radiation Therapy Oncology Group S (2002) Combination chemotherapy and radiotherapy for primary central nervous system lymphoma: radiation therapy oncology group study 93-10. J Clin Oncol 20:4643–4648.  https://doi.org/10.1200/JCO.2002.11.013 CrossRefGoogle Scholar
  4. 4.
    Konovalov AN, Pitskhelauri DI (2003) Principles of treatment of the pineal region tumors. Surg Neurol 59:250–268CrossRefGoogle Scholar
  5. 5.
    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 CrossRefGoogle Scholar
  6. 6.
    Chan AK, Yao Y, Zhang Z, Chung NY, Liu JS, Li KK, Shi Z, Chan DT, Poon WS, Zhou L, Ng HK (2015) TERT promoter mutations contribute to subset prognostication of lower-grade gliomas. Mod Pathol 28:177–186.  https://doi.org/10.1038/modpathol.2014.94 CrossRefGoogle Scholar
  7. 7.
    Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, Pekmezci M, Rice T, Kosel ML, Smirnov IV, Sarkar G, Caron AA, Kollmeyer TM, Praska CE, Chada AR, Halder C, Hansen HM, McCoy LS, Bracci PM, Marshall R, Zheng S, Reis GF, Pico AR, O’Neill BP, Buckner JC, Giannini C, Huse JT, Perry A, Tihan T, Berger MS, Chang SM, Prados MD, Wiemels J, Wiencke JK, Wrensch MR, Jenkins RB (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508.  https://doi.org/10.1056/NEJMoa1407279 CrossRefGoogle Scholar
  8. 8.
    Cancer Genome Atlas Research N, Brat DJ, Verhaak RG, Aldape KD, Yung WK, Salama SR, Cooper LA, Rheinbay E, Miller CR, Vitucci M, Morozova O, Robertson AG, Noushmehr H, Laird PW, Cherniack AD, Akbani R, Huse JT, Ciriello G, Poisson LM, Barnholtz-Sloan JS, Berger MS, Brennan C, Colen RR, Colman H, Flanders AE, Giannini C, Grifford M, Iavarone A, Jain R, Joseph I, Kim J, Kasaian K, Mikkelsen T, Murray BA, O’Neill BP, Pachter L, Parsons DW, Sougnez C, Sulman EP, Vandenberg SR, Van Meir EG, von Deimling A, Zhang H, Crain D, Lau K, Mallery D, Morris S, Paulauskis J, Penny R, Shelton T, Sherman M, Yena P, Black A, Bowen J, Dicostanzo K, Gastier-Foster J, Leraas KM, Lichtenberg TM, Pierson CR, Ramirez NC, Taylor C, Weaver S, Wise L, Zmuda E, Davidsen T, Demchok JA, Eley G, Ferguson ML, Hutter CM, Mills Shaw KR, Ozenberger BA, Sheth M, Sofia HJ, Tarnuzzer R, Wang Z, Yang L, Zenklusen JC, Ayala B, Baboud J, Chudamani S, Jensen MA, Liu J, Pihl T, Raman R, Wan Y, Wu Y, Ally A, Auman JT, Balasundaram M, Balu S, Baylin SB, Beroukhim R, Bootwalla MS, Bowlby R, Bristow CA, Brooks D, Butterfield Y, Carlsen R, Carter S, Chin L, Chu A, Chuah E, Cibulskis K, Clarke A, Coetzee SG, Dhalla N, Fennell T, Fisher S, Gabriel S, Getz G, Gibbs R, Guin R, Hadjipanayis A, Hayes DN, Hinoue T, Hoadley K, Holt RA, Hoyle AP, Jefferys SR, Jones S, Jones CD, Kucherlapati R, Lai PH, Lander E, Lee S, Lichtenstein L, Ma Y, Maglinte DT, Mahadeshwar HS, Marra MA, Mayo M, Meng S, Meyerson ML, Mieczkowski PA, Moore RA, Mose LE, Mungall AJ, Pantazi A, Parfenov M, Park PJ, Parker JS, Perou CM, Protopopov A, Ren X, Roach J, Sabedot TS, Schein J, Schumacher SE, Seidman JG, Seth S, Shen H, Simons JV, Sipahimalani P, Soloway MG, Song X, Sun H, Tabak B, Tam A, Tan D, Tang J, Thiessen N, Triche T Jr, Van Den Berg DJ, Veluvolu U, Waring S, Weisenberger DJ, Wilkerson MD, Wong T, Wu J, Xi L, Xu AW, Yang L, Zack TI, Zhang J, Aksoy BA, Arachchi H, Benz C, Bernard B, Carlin D, Cho J, DiCara D, Frazer S, Fuller GN, Gao J, Gehlenborg N, Haussler D, Heiman DI, Iype L, Jacobsen A, Ju Z, Katzman S, Kim H, Knijnenburg T, Kreisberg RB, Lawrence MS, Lee W, Leinonen K, Lin P, Ling S, Liu W, Liu Y, Liu Y, Lu Y, Mills G, Ng S, Noble MS, Paull E, Rao A, Reynolds S, Saksena G, Sanborn Z, Sander C, Schultz N, Senbabaoglu Y, Shen R, Shmulevich I, Sinha R, Stuart J, Sumer SO, Sun Y, Tasman N, Taylor BS, Voet D, Weinhold N, Weinstein JN, Yang D, Yoshihara K, Zheng S, Zhang W, Zou L, Abel T, Sadeghi S, Cohen ML, Eschbacher J, Hattab EM, Raghunathan A, Schniederjan MJ, Aziz D, Barnett G, Barrett W, Bigner DD, Boice L, Brewer C, Calatozzolo C, Campos B, Carlotti CG Jr, Chan TA, Cuppini L, Curley E, Cuzzubbo S, Devine K, DiMeco F, Duell R, Elder JB, Fehrenbach A, Finocchiaro G, Friedman W, Fulop J, Gardner J, Hermes B, Herold-Mende C, Jungk C, Kendler A, Lehman NL, Lipp E, Liu O, Mandt R, McGraw M, McLendon R, McPherson C, Neder L, Nguyen P, Noss A, Nunziata R, Ostrom QT, Palmer C, Perin A, Pollo B, Potapov A, Potapova O, Rathmell WK, Rotin D, Scarpace L, Schilero C, Senecal K, Shimmel K, Shurkhay V, Sifri S, Singh R, Sloan AE, Smolenski K, Staugaitis SM, Steele R, Thorne L, Tirapelli DP, Unterberg A, Vallurupalli M, Wang Y, Warnick R, Williams F, Wolinsky Y, Bell S, Rosenberg M, Stewart C, Huang F, Grimsby JL, Radenbaugh AJ, Zhang J (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372:2481–2498.  https://doi.org/10.1056/NEJMoa1402121 CrossRefGoogle Scholar
  9. 9.
    Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu CJ, Genovese G, Shmulevich I, Barnholtz-Sloan J, Zou L, Vegesna R, Shukla SA, Ciriello G, Yung WK, Zhang W, Sougnez C, Mikkelsen T, Aldape K, Bigner DD, Van Meir EG, Prados M, Sloan A, Black KL, Eschbacher J, Finocchiaro G, Friedman W, Andrews DW, Guha A, Iacocca M, O’Neill BP, Foltz G, Myers J, Weisenberger DJ, Penny R, Kucherlapati R, Perou CM, Hayes DN, Gibbs R, Marra M, Mills GB, Lander E, Spellman P, Wilson R, Sander C, Weinstein J, Meyerson M, Gabriel S, Laird PW, Haussler D, Getz G, Chin L, Network TR (2013) The somatic genomic landscape of glioblastoma. Cell 155:462–477.  https://doi.org/10.1016/j.cell.2013.09.034 CrossRefGoogle Scholar
  10. 10.
    Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgard G, Solheim O (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 308:1881–1888.  https://doi.org/10.1001/jama.2012.12807 CrossRefGoogle Scholar
  11. 11.
    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 CrossRefGoogle Scholar
  12. 12.
    Bao ZS, Chen HM, Yang MY, Zhang CB, Yu K, Ye WL, Hu BQ, Yan W, Zhang W, Akers J, Ramakrishnan V, Li J, Carter B, Liu YW, Hu HM, Wang Z, Li MY, Yao K, Qiu XG, Kang CS, You YP, Fan XL, Song WS, Li RQ, Su XD, Chen CC, Jiang T (2014) RNA-seq of 272 gliomas revealed a novel, recurrent PTPRZ1-MET fusion transcript in secondary glioblastomas. Genome Res 24:1765–1773.  https://doi.org/10.1101/gr.165126.113 CrossRefGoogle Scholar
  13. 13.
    Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16:284–287.  https://doi.org/10.1089/omi.2011.0118 CrossRefGoogle Scholar
  14. 14.
    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 CrossRefGoogle Scholar
  15. 15.
    McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa AR (2009) Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 110:156–162.  https://doi.org/10.3171/2008.4.17536 CrossRefGoogle Scholar
  16. 16.
    van den Bent MJ, Brandes AA, Taphoorn MJ, Kros JM, Kouwenhoven MC, Delattre JY, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Enting RH, French PJ, Dinjens WN, Vecht CJ, Allgeier A, Lacombe D, Gorlia T, Hoang-Xuan K (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol 31:344–350.  https://doi.org/10.1200/JCO.2012.43.2229 CrossRefGoogle Scholar
  17. 17.
    Cairncross G, Wang M, Shaw E, Jenkins R, Brachman D, Buckner J, Fink K, Souhami L, Laperriere N, Curran W, Mehta M (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 31:337–343.  https://doi.org/10.1200/JCO.2012.43.2674 CrossRefGoogle Scholar
  18. 18.
    Kawaguchi T, Sonoda Y, Shibahara I, Saito R, Kanamori M, Kumabe T, Tominaga T (2016) Impact of gross total resection in patients with WHO grade III glioma harboring the IDH 1/2 mutation without the 1p/19q co-deletion. J Neuro-oncol 129:505–514.  https://doi.org/10.1007/s11060-016-2201-2 CrossRefGoogle Scholar
  19. 19.
    Beiko J, Suki D, Hess KR, Fox BD, Cheung V, Cabral M, Shonka N, Gilbert MR, Sawaya R, Prabhu SS, Weinberg J, Lang FF, Aldape KD, Sulman EP, Rao G, McCutcheon IE, Cahill DP (2014) IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro-oncology 16:81–91.  https://doi.org/10.1093/neuonc/not159 CrossRefGoogle Scholar
  20. 20.
    Wijnenga MMJ, French PJ, Dubbink HJ, Dinjens WNM, Atmodimedjo PN, Kros JM, Smits M, Gahrmann R, Rutten GJ, Verheul JB, Fleischeuer R, Dirven CMF, Vincent A, van den Bent MJ (2018) The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological, and molecular analysis. Neuro-oncology 20:103–112.  https://doi.org/10.1093/neuonc/nox176 CrossRefGoogle Scholar
  21. 21.
    Jakola AS, Skjulsvik AJ, Myrmel KS, Sjavik K, Unsgard G, Torp SH, Aaberg K, Berg T, Dai HY, Johnsen K, Kloster R, Solheim O (2017) Surgical resection versus watchful waiting in low-grade gliomas. Ann Oncol 28:1942–1948.  https://doi.org/10.1093/annonc/mdx230 CrossRefGoogle Scholar
  22. 22.
    Chi AS, Cahill DP, Larvie M, Louis DN (2016) Case 38-2016. A 52-year-old woman with recurrent oligodendroglioma. N Engl J Med 375:2381–2389.  https://doi.org/10.1056/NEJMcpc1610101 CrossRefGoogle Scholar
  23. 23.
    Wang Q, Hu B, Hu X, Kim H, Squatrito M, Scarpace L, deCarvalho AC, Lyu S, Li P, Li Y, Barthel F, Cho HJ, Lin YH, Satani N, Martinez-Ledesma E, Zheng S, Chang E, Sauve CG, Olar A, Lan ZD, Finocchiaro G, Phillips JJ, Berger MS, Gabrusiewicz KR, Wang G, Eskilsson E, Hu J, Mikkelsen T, DePinho RA, Muller F, Heimberger AB, Sulman EP, Nam DH, Verhaak RGW (2017) Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell 32:42–56.e46.  https://doi.org/10.1016/j.ccell.2017.06.003 CrossRefGoogle Scholar
  24. 24.
    Johnson DR, Diehn FE, Giannini C, Jenkins RB, Jenkins SM, Parney IF, Kaufmann TJ (2017) Genetically defined oligodendroglioma is characterized by indistinct tumor borders at MRI. Am J Neuroradiol.  https://doi.org/10.3174/ajnr.A5070 Google Scholar
  25. 25.
    Grossmann P, Gutman DA, Dunn WD Jr, Holder CA, Aerts HJ (2016) Imaging-genomics reveals driving pathways of MRI derived volumetric tumor phenotype features in glioblastoma. BMC Cancer 16:611.  https://doi.org/10.1186/s12885-016-2659-5 CrossRefGoogle Scholar
  26. 26.
    Aibaidula A, Zhao W, Wu JS, Chen H, Shi ZF, Zheng LL, Mao Y, Zhou LF, Sui GD (2016) Microfluidics for rapid detection of isocitrate dehydrogenase 1 mutation for intraoperative application. J Neurosurg 124:1611–1618.  https://doi.org/10.3171/2015.4.JNS141833 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of NeurosurgeryHuashan Hospital, Fudan UniversityShanghaiChina
  2. 2.Beijing Neurosurgical InstituteBeijing Tiantan Hospital, Capital Medical UniversityBeijingChina
  3. 3.Department of NeurosurgeryBeijing Tiantan Hospital, Capital Medical UniversityBeijingChina
  4. 4.Department of NeurosurgeryThe Second Affiliated Hospital of Zhejiang University School of MedicineHangzhouChina
  5. 5.Neurosurgical Immunology LaboratoryNeurosurgical Institute of Fudan UniversityShanghaiChina
  6. 6.Department of PathologyHuashan Hospital, Fudan UniversityShanghaiChina
  7. 7.Department of RadiologyHuashan Hospital, Fudan UniversityShanghaiChina
  8. 8.Department of PathologyBasic Medical Science, Fudan UniversityShanghaiChina
  9. 9.Evidence Based Medicine CenterFudan UniversityShanghaiChina
  10. 10.Department of NeurosurgeryMassachusetts General Hospital, Harvard Medical SchoolBostonUSA
  11. 11.Department of Neuro-Oncology, MD Anderson Cancer CenterUniversity of TexasHoustonUSA

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