Threshold of the extent of resection for WHO Grade III gliomas: retrospective volumetric analysis of 122 cases using intraoperative MRI

Restricted access

OBJECTIVE

WHO Grade III gliomas are relatively rare and treated with multiple modalities such as surgery, chemotherapy, and radiotherapy. The impact of the extent of resection (EOR) on improving survival in patients with this tumor type is unclear. Moreover, because of the heterogeneous radiological appearance of Grade III gliomas, the MRI sequence that best correlates with tumor volume is unknown. In the present retrospective study, the authors evaluated the prognostic significance of EOR.

METHODS

Clinical and radiological data from 122 patients with newly diagnosed WHO Grade III gliomas who had undergone intraoperative MRI–guided resection at a single institution between March 2000 and December 2011 were analyzed retrospectively. Patients were divided into 2 groups by histological subtype: 81 patients had anaplastic astrocytoma (AA) or anaplastic oligoastrocytoma (AOA), and 41 patients had anaplastic oligodendroglioma (AO). EOR was calculated using pre- and postoperative T2-weighted and contrast-enhanced T1-weighted MR images. Univariate and multivariate analyses were performed to evaluate the prognostic significance of EOR on overall survival (OS).

RESULTS

The 5-, 8-, and 10-year OS rates for all patients were 74.28%, 70.59%, and 65.88%, respectively. The 5- and 8-year OS rates for patients with AA and AOA were 72.2% and 67.2%, respectively, and the 10-year OS rate was 62.0%. On the other hand, the 5- and 8-year OS rates for patients with AO were 79.0% and 79.0%; the 10-year OS rate is not yet available. The median pre- and postoperative T2-weighted high–signal intensity volumes were 56.1 cm3 (range 1.3–268 cm3) and 5.9 cm3 (range 0–180 cm3), respectively. The median EOR of T2-weighted high–signal intensity lesions (T2-EOR) and contrast-enhanced T1-weighted lesions were 88.8% (range 0.3%–100%) and 100% (range 34.0%–100%), respectively. A significant survival advantage was associated with resection of 53% or more of the preoperative T2-weighted high–signal intensity volume in patients with AA and AOA, but not in patients with AO. Univariate analysis showed that preoperative Karnofsky Performance Scale score (p = 0.0019), isocitrate dehydrogenase 1 (IDH1) mutation (p = 0.0008), and T2-EOR (p = 0.0208) were significant prognostic factors for survival in patients with AA and AOA. Multivariate analysis demonstrated that T2-EOR (HR 3.28; 95% CI 1.22–8.81; p = 0.0192) and IDH1 mutation (HR 3.90; 95% CI 1.53–10.75; p = 0.0044) were predictive of survival in patients with AA and AOA.

CONCLUSIONS

T2-EOR was one of the most important prognostic factors for patients with AA and AOA. A significant survival advantage was associated with resection of 53% or more of the preoperative T2-weighted high–signal intensity volume in patients with AA and AOA.

ABBREVIATIONS AA = anaplastic astrocytoma; AO = anaplastic oligodendroglioma; AOA = anaplastic oligoastrocytoma; EOR = extent of resection; IDH1 = isocitrate dehydrogenase 1; KPS = Karnofsky Performance Scale; OS = overall survival; RT = radiation therapy; T2-EOR = extent of resection of T2-weighted high–signal intensity lesions; T2-RTV = residual tumor volume of T2-weighted high–signal intensity lesions.
Article Information

Contributor Notes

Correspondence Yoshihiro Muragaki, Faculty of Advanced Techno-Surgery, Institute of Advanced Biomedical Engineering and Science, Tokyo Women’s Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan. email: ymuragaki@twmu.ac.jp.INCLUDE WHEN CITING Published online September 8, 2017; DOI: 10.3171/2017.3.JNS162383.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings
References
  • 1

    Beiko JSuki DHess KRFox BDCheung VCabral M: IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro Oncol 16:81912014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Belhawi SMKHoefnagels FWABaaijen JCAliaga ESReijneveld JCHeimans JJ: Early postoperative MRI overestimates residual tumour after resection of gliomas with no or minimal enhancement. Eur Radiol 21:152615342011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Chaichana KLJusue-Torres INavarro-Ramirez RRaza SMPascual-Gallego MIbrahim A: Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16:1131222014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Chaichana KLKosztowski TNiranjan AOlivi AWeingart JDLaterra J: Prognostic significance of contrast-enhancing anaplastic astrocytomas in adults. J Neurosurg 113:2862922010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Fukui AMuragaki YSaito TMaruyama TNitta MIkuta S: Volumetric analysis using low-field intraoperative magnetic resonance imaging for 168 newly diagnosed supratentorial glioblastomas: effects of extent of resection and residual tumor volume on survival and recurrence. World Neurosurg 98:73802017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Glass JHochberg FHGruber MLLouis DNSmith DRattner B: The treatment of oligodendrogliomas and mixed oligodendroglioma-astrocytomas with PCV chemotherapy. J Neurosurg 76:7417451992

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Grabowski MMRecinos PFNowacki ASSchroeder JLAngelov LBarnett GH: Residual tumor volume versus extent of resection: predictors of survival after surgery for glioblastoma. J Neurosurg 121:111511232014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Iseki HNakamura RMuragaki YSuzuki TChernov MHori T: Advanced computer-aided intraoperative technologies for information-guided surgical management of gliomas: Tokyo Women’s Medical University experience. Minim Invasive Neurosurg 51:2852912008

    • PubMed
    • Export Citation
  • 9

    Keles GEChang EFLamborn KRTihan TChang CJChang SM: Volumetric extent of resection and residual contrast enhancement on initial surgery as predictors of outcome in adult patients with hemispheric anaplastic astrocytoma. J Neurosurg 105:34402006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kim WLiau LM: IDH mutations in human glioma. Neurosurg Clin N Am 23:4714802012

  • 11

    Kubben PLter Meulen KJSchijns OEMGter Laak-Poort MPvan Overbeeke JJvan Santbrink H: Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 12:106210702011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lacroix MAbi-Said DFourney DRGokaslan ZLShi WDeMonte F: A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:1901982001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Li YMSuki DHess KSawaya R: The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection? J Neurosurg 124:9779882016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Louis DNOhgaki HWiestler ODCavenee WK: WHO Classification of Tumours of the Central Nervous Systemed 4. Lyon: IARC Press2007

    • PubMed
    • Export Citation
  • 15

    Louis DNOhgaki HWiestler ODCavenee WK: WHO Classification of Tumours of the Central Nervous Systemed 4 revised. Lyon: IARC Press2016

    • Export Citation
  • 16

    Mohammadi AMSullivan TBBarnett GHRecinos VAngelov LKamian K: Use of high-field intraoperative magnetic resonance imaging to enhance the extent of resection of enhancing and nonenhancing gliomas. Neurosurgery 74:3393502014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Muragaki YIseki HMaruyama TTanaka MShinohara CSuzuki T: Information-guided surgical management of gliomas using low-field-strength intraoperative MRI. Acta Neurochir Suppl 109:67722011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Nitta MMuragaki YMaruyama TIkuta SKomori TMaebayashi K: Proposed therapeutic strategy for adult low-grade glioma based on aggressive tumor resection. Neurosurg Focus 38(1):E72015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Nomiya TNemoto KKumabe TTakai YYamada S: Prognostic significance of surgery and radiation therapy in cases of anaplastic astrocytoma: retrospective analysis of 170 cases. J Neurosurg 106:5755812007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Nuño MBirch KMukherjee DSarmiento JMBlack KLPatil CG: Survival and prognostic factors of anaplastic gliomas. Neurosurgery 73:4584652013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Ostrom QTGittleman HFulop JLiu MBlanda RKromer C: CBTRUS Statistical Report: Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2008–2012. Neuro Oncol 17 (Suppl 4):iv1iv622015

    • Search Google Scholar
    • Export Citation
  • 22

    Padwal JADong XHirshman BRHoi-Sang UCarter BSChen CC: Superior efficacy of gross total resection in anaplastic astrocytoma patients relative to glioblastoma patients. World Neurosurg 90:1861932016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Pala ABrand CKapapa THlavac MKönig RSchmitz B: The value of intraoperative and early postoperative magnetic resonance imaging in low-grade glioma surgery: a retrospective study. World Neurosurg 93:1911972016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Pessina FNavarria PCozzi LAscolese AMSimonelli MSantoro A: Value of surgical resection in patients with newly diagnosed Grade III glioma treated in a multimodal approach: surgery, chemotherapy and radiotherapy. Ann Surg Oncol 23:304030462016

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Puduvalli VKHashmi MMcAllister LDLevin VAHess KRPrados M: Anaplastic oligodendrogliomas: prognostic factors for tumor recurrence and survival. Oncology 65:2592662003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Saito TMaruyama TMuragaki YTanaka MNitta MShinoda J: 11C-methionine uptake correlates with combined 1p and 19q loss of heterozygosity in oligodendroglial tumors. AJNR Am J Neuroradiol 34:85912013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Saito TMuragaki YMaruyama TKomori TTamura MNitta M: Calcification on CT is a simple and valuable preoperative indicator of 1p/19q loss of heterozygosity in supratentorial brain tumors that are suspected grade II and III gliomas. Brain Tumor Pathol 33:1751822016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Sanai NBerger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753–7642642662008

  • 29

    Sanai NPolley MYMcDermott MWParsa ATBerger MS: An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:382011

  • 30

    Senft CBink AFranz KVatter HGasser TSeifert V: Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:99710032011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Shirai KSuzuki YOkamoto MWakatsuki MNoda SETakahashi T: Influence of histological subtype on survival after combined therapy of surgery and radiation in WHO grade 3 glioma. J Radiat Res (Tokyo) 51:5895942010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Smith JSChang EFLamborn KRChang SMPrados MDCha S: Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:133813452008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Tortosa AViñolas NVillà SVerger EGil JMBrell M: Prognostic implication of clinical, radiologic, and pathologic features in patients with anaplastic gliomas. Cancer 97:106310712003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Vuorinen VHinkka SFärkkilä MJääskeläinen J: Debulking or biopsy of malignant glioma in elderly people — a randomised study. Acta Neurochir (Wien) 145:5102003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Wang YWang KWang JLi SMa JDai J: Identifying the association between contrast enhancement pattern, surgical resection, and prognosis in anaplastic glioma patients. Neuroradiology 58:3673742016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
TrendMD
Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 500 491 117
Full Text Views 366 208 10
PDF Downloads 208 116 10
EPUB Downloads 0 0 0
PubMed
Google Scholar