Intraoperative MRI for newly diagnosed supratentorial glioblastoma: a multicenter-registry comparative study to conventional surgery

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  • 1 Department of Neurosurgery, Washington University School of Medicine, St. Louis, Missouri;
  • 2 Department of Radiology, University of Minnesota, Minneapolis, Minnesota;
  • 3 Allina Health, Minneapolis, Minnesota;
  • 4 Department of Neurosurgery, Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah;
  • 5 Department of Clinical Sciences and Hotchkiss Brain Institute, University of Calgary, Alberta, Canada;
  • 6 Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts;
  • 7 Department of Neurosurgery, St. Thomas Hospital, Nashville, Tennessee;
  • 8 Department of Neurosurgery, Cook Children’s Hospital, Fort Worth, Texas; and
  • 9 Department of Neurological Surgery, Goodman Campbell and Indiana University, Indianapolis, Indiana
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OBJECTIVE

Intraoperative MRI (iMRI) is used in the surgical treatment of glioblastoma, with uncertain effects on outcomes. The authors evaluated the impact of iMRI on extent of resection (EOR) and overall survival (OS) while controlling for other known and suspected predictors.

METHODS

A multicenter retrospective cohort of 640 adult patients with newly diagnosed supratentorial glioblastoma who underwent resection was evaluated. iMRI was performed in 332/640 cases (51.9%). Reviews of MRI features and tumor volumetric analysis were performed on a subsample of cases (n = 286; 110 non-iMRI, 176 iMRI) from a single institution.

RESULTS

The median age was 60.0 years (mean 58.5 years, range 20.5–86.3 years). The median OS was 17.0 months (95% CI 15.6–18.4 months). Gross-total resection (GTR) was achieved in 403/640 cases (63.0%). Kaplan-Meier analysis of 286 cases with volumetric analysis for EOR (grouped into 100%, 95%–99%, 80%–94%, and 50%–79%) showed longer OS for 100% EOR compared to all other groups (p < 0.01). Additional resection after iMRI was performed in 104/122 cases (85.2%) with initial subtotal resection (STR), leading to a 6.3% mean increase in EOR and a 2.2-cm3 mean decrease in tumor volume. For iMRI cases with volumetric analysis, the GTR rate increased from 54/176 (30.7%) on iMRI to 126/176 (71.5%) postoperatively. The EOR was significantly higher in the iMRI group for intended GTR and STR groups (p = 0.02 and p < 0.01, respectively). Predictors of GTR on multivariate logistic regression included iMRI use and intended GTR. Predictors of shorter OS on multivariate Cox regression included older age, STR, isocitrate dehydrogenase 1 (IDH1) wild type, no O 6-methylguanine DNA methyltransferase (MGMT) methylation, and no Stupp therapy. iMRI was a significant predictor of OS on univariate (HR 0.82, 95% CI 0.69–0.98; p = 0.03) but not multivariate analyses. Use of iMRI was not associated with an increased rate of new permanent neurological deficits.

CONCLUSIONS

GTR increased OS for patients with newly diagnosed glioblastoma after adjusting for other prognostic factors. iMRI increased EOR and GTR rate and was a significant predictor of GTR on multivariate analysis; however, iMRI was not an independent predictor of OS. Additional supporting evidence is needed to determine the clinical benefit of iMRI in the management of glioblastoma.

ABBREVIATIONS ASA = American Society of Anesthesiologists; EOR = extent of resection; GTR = gross-total resection; IDH = isocitrate dehydrogenase; I-MiND = IMRIS Multicenter iMRI Neurosurgery Database; iMRI = intraoperative MRI; iUS = intraoperative ultrasound; KPS = Karnofsky Performance Scale; MGMT = O6-methylguanine DNA methyltransferase; nPND = new permanent neurological deficits; OS = overall survival; PFS = progression-free survival; QALY = quality-adjusted life year; STR = subtotal resection; 5-ALA = 5-aminolevulinic acid.

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Contributor Notes

Correspondence Michael R. Chicoine: Washington University School of Medicine, St. Louis, MO. chicoinem@wudosis.wustl.edu.

INCLUDE WHEN CITING Published online October 9, 2020; DOI: 10.3171/2020.6.JNS19287.

Disclosures Dr. Chicoine received funding from the following sources: 1) IMRIS, Inc., for an unrestricted educational grant to support an iMRI database and outcomes analysis project, the IMRIS Multicenter intraoperative MRI Neurosurgery Database (I-MiND); 2) The Head for the Cure Foundation; and 3) Mrs. Carol Rossfeld and The Alex & Alice Aboussie Family Charitable Foundation. REDCap database supported by Clinical and Translational Science Award (CTSA) Grant [UL1 TR000448] and Siteman Comprehensive Cancer Center and NCI Cancer Center Support Grant P30 CA091842. Dr. Dunn is a cofounder with equity in Immunovalent. Dr. Jensen is a consultant for Medtronic. Dr. Kim is a consultant for Monteris Medical and receives support of non–study-related clinical or research effort that he oversees from Monteris Medical, Stryker, and Collagen Matrix. Dr. Leuthardt has direct stock ownership in Neurolutions, Sora Imaging Solutions, Osteovantage, Immunovalent, Inner Cosmos, Face to Face Biometrics, and Caeli Vascular. He is a consultant for Monteris and Sante Ventures. Dr. Oswood is in the speakers’ bureau for Philips Healthcare. The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.

  • 1

    Ostrom QT, Gittleman H, Liao P, CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro Oncol. 2014;16(suppl 4):iv1iv63.

    • Search Google Scholar
    • Export Citation
  • 2

    Pan IW, Ferguson SD, Lam S. Patient and treatment factors associated with survival among adult glioblastoma patients: a USA population-based study from 2000–2010. J Clin Neurosci. 2015;22(10):15751581.

    • Search Google Scholar
    • Export Citation
  • 3

    Stupp R, Hegi ME, Mason WP, Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459466.

    • Search Google Scholar
    • Export Citation
  • 4

    Stupp R, Mason WP, van den Bent MJ, Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987996.

    • Search Google Scholar
    • Export Citation
  • 5

    Woehrer A, Bauchet L, Barnholtz-Sloan JS. Glioblastoma survival: has it improved? Evidence from population-based studies. Curr Opin Neurol. 2014;27(6):666674.

    • Search Google Scholar
    • Export Citation
  • 6

    Lacroix M, Abi-Said D, Fourney DR, A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg. 2001;95(2):190198.

    • Search Google Scholar
    • Export Citation
  • 7

    Mineo JF, Bordron A, Baroncini M, Prognosis factors of survival time in patients with glioblastoma multiforme: a multivariate analysis of 340 patients. Acta Neurochir (Wien). 2007;149(3):245253.

    • Search Google Scholar
    • Export Citation
  • 8

    Yan H, Parsons DW, Jin G, IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360(8):765773.

  • 9

    Beiko J, Suki D, Hess KR, IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro Oncol. 2014;16(1):8191.

    • Search Google Scholar
    • Export Citation
  • 10

    Miller JJ, Shih HA, Andronesi OC, Cahill DP. Isocitrate dehydrogenase-mutant glioma: evolving clinical and therapeutic implications. Cancer. 2017;123(23):45354546.

    • Search Google Scholar
    • Export Citation
  • 11

    Cao VT, Jung TY, Jung S, The correlation and prognostic significance of MGMT promoter methylation and MGMT protein in glioblastomas. Neurosurgery. 2009;65(5):866875.

    • Search Google Scholar
    • Export Citation
  • 12

    Hegi ME, Diserens AC, Gorlia T, MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):9971003.

    • Search Google Scholar
    • Export Citation
  • 13

    Louis DN, Perry A, Reifenberger G, The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol. 2016;131(6):803820.

    • Search Google Scholar
    • Export Citation
  • 14

    Sanai N, Polley MY, McDermott MW, An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg. 2011;115(1):38.

  • 15

    Brown TJ, Brennan MC, Li M, Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol. 2016;2(11):14601469.

    • Search Google Scholar
    • Export Citation
  • 16

    Li YM, Suki D, Hess K, Sawaya R. The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection? J Neurosurg. 2016;124(4):977988.

    • Search Google Scholar
    • Export Citation
  • 17

    Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62(4):753–764, 264266.

  • 18

    Nimsky C, Ganslandt O, Von Keller B, Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology. 2004;233(1):6778.

    • Search Google Scholar
    • Export Citation
  • 19

    Chicoine MR, Lim CC, Evans JA, Implementation and preliminary clinical experience with the use of ceiling mounted mobile high field intraoperative magnetic resonance imaging between two operating rooms. Acta Neurochir Suppl. 2011;109:97102.

    • Search Google Scholar
    • Export Citation
  • 20

    Haydon DH, Chicoine MR, Dacey RG Jr. The impact of high-field-strength intraoperative magnetic resonance imaging on brain tumor management. Neurosurgery. 2013;60(suppl 1):9297.

    • Search Google Scholar
    • Export Citation
  • 21

    Kubben PL, ter Meulen KJ, Schijns OE, Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol. 2011;12(11):10621070.

    • Search Google Scholar
    • Export Citation
  • 22

    Li P, Qian R, Niu C, Fu X. Impact of intraoperative MRI-guided resection on resection and survival in patient with gliomas: a meta-analysis. Curr Med Res Opin. 2017;33(4):621630.

    • Search Google Scholar
    • Export Citation
  • 23

    Senft C, Bink A, Franz K, Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol. 2011;12(11):9971003.

    • Search Google Scholar
    • Export Citation
  • 24

    Kubben PL, Scholtes F, Schijns OE, Intraoperative magnetic resonance imaging versus standard neuronavigation for the neurosurgical treatment of glioblastoma: a randomized controlled trial. Surg Neurol Int. 2014;5:70.

    • Search Google Scholar
    • Export Citation
  • 25

    Jenkinson MD, Barone DG, Bryant A, Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev. 2018;1:CD012788.

    • Search Google Scholar
    • Export Citation
  • 26

    Coburger J, Merkel A, Scherer M, Low-grade glioma surgery in intraoperative magnetic resonance imaging: results of a multicenter retrospective assessment of the German Study Group for Intraoperative Magnetic Resonance Imaging. Neurosurgery. 2016;78(6):775786.

    • Search Google Scholar
    • Export Citation
  • 27

    Harris PA, Taylor R, Thielke R, Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377381.

    • Search Google Scholar
    • Export Citation
  • 28

    Sylvester PT, Evans JA, Zipfel GJ, Combined high-field intraoperative magnetic resonance imaging and endoscopy increase extent of resection and progression-free survival for pituitary adenomas. Pituitary. 2015;18(1):7285.

    • Search Google Scholar
    • Export Citation
  • 29

    Reponen E, Tuominen H, Korja M. Evidence for the use of preoperative risk assessment scores in elective cranial neurosurgery: a systematic review of the literature. Anesth Analg. 2014;119(2):420432.

    • Search Google Scholar
    • Export Citation
  • 30

    Young J, Badgery-Parker T, Dobbins T, Comparison of ECOG/WHO performance status and ASA score as a measure of functional status. J Pain Symptom Manage. 2015;49(2):258264.

    • Search Google Scholar
    • Export Citation
  • 31

    Kikinis R, Pieper SD, Vosburgh KG. 3D Slicer: a platform for subject-specific image analysis, visualization, and clinical support. In: Jolesz FA, ed. Intraoperative Imaging and Image-Guided Therapy. Springer New York; 2014:277289.

    • Search Google Scholar
    • Export Citation
  • 32

    Trifiletti DM, Alonso C, Grover S, Prognostic implications of extent of resection in glioblastoma: analysis from a large database. World Neurosurg. 2017;103:330340.

    • Search Google Scholar
    • Export Citation
  • 33

    Kuhnt D, Becker A, Ganslandt O, Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol. 2011;13(12):13391348.

    • Search Google Scholar
    • Export Citation
  • 34

    Coburger J, Segovia von Riehm J, Ganslandt O, Is there an indication for intraoperative MRI in subtotal resection of glioblastoma? A multicenter retrospective comparative analysis. World Neurosurg. 2018;110:e389e397.

    • Search Google Scholar
    • Export Citation
  • 35

    Rahman M, Abbatematteo J, De Leo EK, The effects of new or worsened postoperative neurological deficits on survival of patients with glioblastoma. J Neurosurg. 2017;127(1):123131.

    • Search Google Scholar
    • Export Citation
  • 36

    Stummer W, Pichlmeier U, Meinel T, Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7(5):392401.

    • Search Google Scholar
    • Export Citation
  • 37

    Roder C, Bisdas S, Ebner FH, Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol. 2014;40(3):297304.

    • Search Google Scholar
    • Export Citation
  • 38

    Coburger J, Hagel V, Wirtz CR, König R. Surgery for glioblastoma: impact of the combined use of 5-aminolevulinic acid and intraoperative MRI on extent of resection and survival. PLoS One. 2015;10(6):e0131872.

    • Search Google Scholar
    • Export Citation
  • 39

    Coburger J, Scheuerle A, Kapapa T, Sensitivity and specificity of linear array intraoperative ultrasound in glioblastoma surgery: a comparative study with high field intraoperative MRI and conventional sector array ultrasound. Neurosurg Rev. 2015;38(3):499509.

    • Search Google Scholar
    • Export Citation
  • 40

    Eljamel MS, Mahboob SO. The effectiveness and cost-effectiveness of intraoperative imaging in high-grade glioma resection; a comparative review of intraoperative ALA, fluorescein, ultrasound and MRI. Photodiagn Photodyn Ther. 2016;16:3543.

    • Search Google Scholar
    • Export Citation
  • 41

    Abraham P, Sarkar R, Brandel MG, Cost-effectiveness of intraoperative MRI for treatment of high-grade gliomas. Radiology. 2019;291(3):689697.

    • Search Google Scholar
    • Export Citation
  • 42

    McGirt MJ, Speroff T, Dittus RS, The National Neurosurgery Quality and Outcomes Database (N2QOD): general overview and pilot-year project description. Neurosurg Focus. 2013;34(1):E6.

    • Search Google Scholar
    • Export Citation
  • 43

    Henker C, Hiepel MC, Kriesen T, Volumetric assessment of glioblastoma and its predictive value for survival. Acta Neurochir (Wien). 2019;161(8):17231732.

    • Search Google Scholar
    • Export Citation
  • 44

    Zhang Z, Jiang H, Chen X, Identifying the survival subtypes of glioblastoma by quantitative volumetric analysis of MRI. J Neurooncol. 2014;119(1):207214.

    • Search Google Scholar
    • Export Citation
  • 45

    Molinaro AM, Hervey-Jumper S, Morshed RA, 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. 2020;6(4):495503.

    • Search Google Scholar
    • Export Citation

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