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Open Access 01-10-2017 | Original Article

Predicting surgical outcome in patients with glioblastoma multiforme using pre-operative magnetic resonance imaging: development and preliminary validation of a grading system

Authors: Hani J. Marcus, Sophie Williams, Archie Hughes-Hallett, Sophie J. Camp, Dipankar Nandi, Lewis Thorne

Published in: Neurosurgical Review | Issue 4/2017

Abstract

The lack of a simple, objective and reproducible system to describe glioblastoma multiforme (GBM) represents a major limitation in comparative effectiveness research. The objectives of this study were therefore to develop such a grading system and to validate it on patients who underwent surgical resection. A systematic review of the literature was performed to identify features on pre-operative magnetic resonance imaging (MRI) that predict the surgical outcome of patients with GBM. In all, the five most important features of GBM on pre-operative MRI were as follows: periventricular or deep location, corpus callosum or bilateral location, eloquent location, size and associated oedema. These were then used to develop a grading system. To validate this grading system, a retrospective cohort study of all adult patients with supratentorial GBM who underwent surgical resection between the 1 January 2014 and the 31 June 2015 was performed. There was a substantial agreement between the two neurosurgeons grading GBM (Cohen’s κ was 0.625; standard error 0.066). High-complexity lesions were significantly less likely to result in complete resection of contrast-enhancing tumour than low-complexity lesions (50.0 versus 3.4%; p = 0.0007). The proposed grading system may allow for the standardised communication of anatomical features of GBM identified on pre-operative MRI.

Adeberg S, Bostel T, Konig L, Welzel T, Debus J, Combs SE (2014) A comparison of long-term survivors and short-term survivors with glioblastoma, subventricular zone involvement: a predictive factor for survival? Radiat Oncol 9:95. doi:10.1186/1748-717X-9-95 CrossRefPubMedPubMedCentral

Balog J, Sasi-Szabo L, Kinross J, Lewis MR, Muirhead LJ, Veselkov K, Mirnezami R, Dezso B, Damjanovich L, Darzi A et al (2013) Intraoperative tissue identification using rapid evaporative ionization mass spectrometry. Sci Transl Med 5. doi:10.1126/scitranslmed.3005623

Barone DG, Lawrie TA, Hart MG (2014) Image guided surgery for the resection of brain tumours. Cochrane Database Syst Rev 1:CD009685. doi:10.1002/14651858.CD009685.pub2

Benveniste R, Germano IM (2003) Evaluation of factors predicting accurate resection of high-grade gliomas by using frameless image-guided stereotactic guidance. Neurosurg Focus 14(2):e5CrossRefPubMed

Bodily L, Mintz AH, Engh J (2013) Combined awake craniotomy with endoscopic port surgery for resection of a deep-seated temporal lobe glioma: a case report. Case Rep Med 2013:401359. doi:10.1155/2013/401359 CrossRefPubMedPubMedCentral

Chaichana KL, McGirt MJ, Frazier J, Attenello F, Guerrero-Cazares H, Quinones-Hinojosa A (2008) Relationship of glioblastoma multiforme to the lateral ventricles predicts survival following tumor resection. J Neurooncol 89(2):219–224

Chaichana K, Parker S, Olivi A, Quinones-Hinojosa A (2010) A proposed classification system that projects outcomes based on preoperative variables for adult patients with glioblastoma multiforme. J Neurosurg 112(5):997–1004. doi:10.3171/2009.9.JNS09805 CrossRefPubMed

Chaichana KL, Chaichana KK, Olivi A, Weingart JD, Bennett R, Brem H, Quinones-Hinojosa A (2011) Surgical outcomes for older patients with glioblastoma multiforme: preoperative factors associated with decreased survival. Clinical article. J Neurosurg 114(3):587–594. doi:10.3171/2010.8.JNS1081 CrossRefPubMed

Chaichana KL, Pendleton C, Chambless L, Camara-Quintana J, Nathan JK, Hassam-Malani L, Li G, Harsh GR IV, Thompson RC, Lim M, Quinones-Hinojosa (2013a) A Multi-institutional validation of a preoperative scoring system which predicts survival for patients with glioblastoma. J Clin Neurosci 20(10):1422–1426

10.

Chaichana KL, Martinez-Gutierrez JC, De la Garza-Ramos R, Weingart JD, Olivi A, Gallia GL, Lim M, Brem H, Quinones-Hinojosa A (2013b) Factors associated with survival for patients with glioblastoma with poor pre-operative functional status. J Clin Neurosci 20(6):818–823. doi:10.1016/j.jocn.2012.07.016 CrossRefPubMedPubMedCentral

11.

Chen KT, Wu TW, Chuang CC, Hsu YH, Hsu PW, Huang YC, Lin TK, Chang CN, Lee ST, Wu CT et al (2015) Corpus callosum involvement and postoperative outcomes of patients with gliomas. J Neuro-Oncol 124(2):207–214. doi:10.1007/s11060-015-1823-0 CrossRef

12.

Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C et al (2009) The Clavien-Dindo classification of surgical complications five-year experience. Ann Surg 250:187–196. doi:10.1097/SLA.0b013e3181b13ca2 CrossRefPubMed

13.

Cook JA, McCulloch P, Blazeby JM, Beard DJ, Marinac-Dabic D, Sedrakyan A, Grp I (2013) IDEAL framework for surgical innovation 3: randomised controlled trials in the assessment stage and evaluations in the long term study stage. Bmj-British Medical Journal 346. doi:10.1136/Bmj.F2820

14.

Dandy WE (1928) Removal of right cerebral hemisphere for certain tumors with hemiplegia. JAMA 90:823–825CrossRef

15.

Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications—a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213. doi:10.1097/01.sla.0000133083.54934.ae CrossRefPubMedPubMedCentral

16.

Durmaz R, Erken S, Arslantas A, Atasoy MA, Bal C, Tel E (1997) Management of glioblastoma multiforme: with special reference to recurrence. Clin Neurol Neurosurg 99(2):117–123CrossRefPubMed

17.

Ergina PL, Barkun JS, McCulloch P, Cook JA, Altman DG, Grp I (2013) IDEAL framework for surgical innovation 2: observational studies in the exploration assessment stages. Bmj-British Medical Journal 346. doi:10.1136/Bmj.F3011

18.

Fernandez-Miranda JC, Engh JA, Pathak SK, Madhok R, Boada FE, Schneider W, Kassam AB (2010) High-definition fiber tracking guidance for intraparenchymal endoscopic port surgery. J Neurosurg 113:990–999. doi:10.3171/2009.10.JNS09933 CrossRefPubMed

19.

Foersch S, Heimann A, Ayyad A, Spoden GA, Florin L, Mpoukouvalas K, Kiesslich R, Kempski O, Goetz M, Charalampaki P (2012) Confocal laser endomicroscopy for diagnosis and histomorphologic imaging of brain tumors in vivo. PLoS One 7:e41760. doi:10.1371/journal.pone.0041760 CrossRefPubMedPubMedCentral

20.

Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Lango T, Unsgard G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47:1373–1379 discussion 1379-1380CrossRefPubMed

21.

Hammoud MA, Sawaya R, Shi W, Thall PF, Leeds NE (1996) Prognostic significance of preoperative MRI scans in glioblastoma multiforme. J Neurooncol 27(1):65–73CrossRefPubMed

22.

Helseth R, Helseth E, Johannesen TB, Langberg CW, Lote K, Ronning P, Scheie D, Vik A, Meling TR (2010) Overall survival, prognostic factors, and repeated surgery in a consecutive series of 516 patients with glioblastoma multiforme. Acta Neurol Scand 122(3):159–167. doi:10.1111/j.1600-0404.2010.01350.x CrossRefPubMed

23.

Jain R, Poisson LM, Gutman D, Scarpace L, Hwang SN, Holder CA, Wintermark M, Rao A, Colen RR, Kirby J, Freymann J, Jaffe CC, Mikkelsen T, Flanders A (2014) Outcome prediction in patients with glioblastoma by using imaging, clinical, and genomic biomarkers: focus on the nonenhancing component of the tumor. Radiology 272(2):484–493

24.

Jermyn M, Mok K, Mercier J, Desroches J, Pichette J, Saint-Arnaud K, Bernstein L, Guiot MC, Petrecca K, Leblond F (2015) Intraoperative brain cancer detection with Raman spectroscopy in humans. Sci Transl Med 7. doi:10.1126/scitranslmed.aaa2384

25.

Konglund A, Helseth R, Lund-Johansen M, Helseth E, Meling TR (2013) Surgery for high-grade gliomas in the aging. Acta Neurol Scand 128(3):185–193

26.

Kubben PL, ter Meulen KJ, Schijns OEMG, ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H (2011) Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 12:1062–1070. doi:10.1016/S1470-2045(11)70130-9 CrossRefPubMed

27.

Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E et al (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95(2):190–198. doi:10.3171/jns.2001.95.2.0190 CrossRefPubMed

28.

Li SW, Qiu XG, Chen BS, Zhang W, Ren H, Wang ZC, Jiang T (2009) Prognostic factors influencing clinical outcomes of glioblastoma multiforme. Chin Med J (Engl) 122(11):1245–1249

29.

Li YM, Suki D, Hess K, Sawaya R (2016) The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection? J Neurosurg 124:977–988. doi:10.3171/2015.5.JNS142087 CrossRefPubMed

30.

Ma X, Lv Y, Liu J, Wang D, Huang Q, Wang X, Li G, Xu S, Li X (2009) Survival analysis of 205 patients with glioblastoma multiforme: clinical characteristics, treatment and prognosis in China. J Clin Neurosci 16(12):1595–1598. doi:10.1016/j.jocn.2009.02.036 CrossRefPubMed

31.

McCulloch P, Cook JA, Altman DG, Heneghan C, Diener MK, Grp I (2013) IDEAL framework for surgical innovation 1: the idea and development stages. Bmj-British Medical Journal 346. doi:10.1136/Bmj.F3012

32.

Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement. BMJ 339:b2535. doi:10.1136/bmj.b2535 CrossRefPubMedPubMedCentral

33.

Park JK, Hodges T, Arko L, Shen M, Dello Iacono D, McNabb A, Olsen Bailey N, Kreisl TN, Iwamoto FM, Sul J et al (2010) Scale to predict survival after surgery for recurrent glioblastoma multiforme. J Clin Oncol 28(24):3838–3843. doi:10.1200/JCO.2010.30.0582 CrossRefPubMedPubMedCentral

34.

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. doi:10.3171/2011.2.JNS1099810.3171/2011.7.JNS10238 CrossRefPubMed

35.

Schoenegger K, Oberndorfer S, Wuschitz B, Struhal W, Hainfellner J, Prayer D, Heinzl H, Lahrmann H, Marosi C, Grisold W (2009) Peritumoral edema on MRI at initial diagnosis: an independent prognostic factor for glioblastoma? Eur J Neurol 16(7):874–878. doi:10.1111/j.1468-1331.2009.02613.x CrossRefPubMed

36.

Schucht P, Beck J, Abu-Isa J, Andereggen L, Murek M, Seidel K, Stieglitz L, Raabe A (2012) Gross total resection rates in contemporary glioblastoma surgery: results of an institutional protocol combining 5-aminolevulinic acid intraoperative fluorescence imaging and brain mapping. Neurosurgery 71:927–935 . doi:10.1227/NEU.0b013e31826d1e6bdiscussion 935-926CrossRefPubMed

37.

Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65:476–483CrossRefPubMed

38.

Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, Group AL-GS (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401. doi:10.1016/S1470-2045(06)70665-9 CrossRefPubMed

39.

Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C et al (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62(3):564–576 . doi:10.1227/01.neu.0000317304.31579.17 discussion 564–576CrossRefPubMed

40.

Taylor MD, Bernstein M (1999) Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. J Neurosurg 90:35–41. doi:10.3171/jns.1999.90.1.0035 CrossRefPubMed

41.

Tejada-Solis S, Aldave-Orzaiz G, Pay-Valverde E, Marigil-Sanchez M, Idoate-Gastearena MA, Diez-Valle R (2012) Prognostic value of ventricular wall fluorescence during 5-aminolevulinic-guided surgery for glioblastoma. Acta Neurochir Wien 154(11):1997–2002

42.

von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457. doi:10.1016/S0140-6736(07)61602-X CrossRef

43.

Vuorinen V, Hinkka S, Farkkila M, Jaaskelainen J (2003) Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir 145:5–10. doi:10.1007/s00701-002-1030-6 CrossRefPubMed

Title: Predicting surgical outcome in patients with glioblastoma multiforme using pre-operative magnetic resonance imaging: development and preliminary validation of a grading system
Authors: Hani J. Marcus
Sophie Williams
Archie Hughes-Hallett
Sophie J. Camp
Dipankar Nandi
Lewis Thorne
Publication date: 01-10-2017
Publisher: Springer Berlin Heidelberg
Published in: Neurosurgical Review / Issue 4/2017
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI: https://doi.org/10.1007/s10143-017-0817-0

Keynote webinar | Spotlight on sleep in brain health

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Predicting surgical outcome in patients with glioblastoma multiforme using pre-operative magnetic resonance imaging: development and preliminary validation of a grading system

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

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