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Published in: Journal of Neuro-Oncology 2/2019

01-06-2019 | Glioma | Clinical Study

Evaluation of pediatric glioma outcomes using intraoperative MRI: a multicenter cohort study

Authors: Michael Karsy, S. Hassan Akbari, David Limbrick, Eric C. Leuthardt, John Evans, Matthew D. Smyth, Jennifer Strahle, Jeffrey Leonard, Samuel Cheshier, Douglas L. Brockmeyer, Robert J. Bollo, John R. Kestle, John Honeycutt, David J. Donahue, Richard A. Roberts, Daniel R. Hansen, Jay Riva-Cambrin, Garnette Sutherland, Clair Gallagher, Walter Hader, Yves Starreveld, Mark Hamilton, Ann-Christine Duhaime, Randy L. Jensen, Michael R. Chicoine

Published in: Journal of Neuro-Oncology | Issue 2/2019

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Abstract

Background

The use of intraoperative MRI (iMRI) during treatment of gliomas may increase extent of resection (EOR), decrease need for early reoperation, and increase progression-free and overall survival, but has not been fully validated, particularly in the pediatric population.

Objective

To assess the accuracy of iMRI to identify residual tumor in pediatric patients with glioma and determine the effect of iMRI on decisions for resection, complication rates, and other outcomes.

Methods

We retrospectively analyzed a multicenter database of pediatric patients (age ≤ 18 years) who underwent resection of pathologically confirmed gliomas.

Results

We identified 314 patients (mean age 9.7 ± 4.6 years) with mean follow-up of 48.3 ± 33.6 months (range 0.03–182.07 months) who underwent surgery with iMRI. There were 201 (64.0%) WHO grade I tumors, 57 (18.2%) grade II, 24 (7.6%) grade III, 9 (2.9%) grade IV, and 23 (7.3%) not classified. Among 280 patients who underwent resection using iMRI, 131 (46.8%) had some residual tumor and underwent additional resection after the first iMRI. Of the 33 tissue specimens sent for pathological analysis after iMRI, 29 (87.9%) showed positive tumor pathology. Gross total resection was identified in 156 patients (55.7%), but this was limited by 69 (24.6%) patients with unknown EOR.

Conclusions

Analysis of the largest multicenter database of pediatric gliomas resected using iMRI demonstrated additional tumor resection in a substantial portion of cases. However, determining the impact of iMRI on EOR and outcomes remains challenging because iMRI use varies among providers nationally. Continued refinement of iMRI techniques for use in pediatric patients with glioma may improve outcomes.
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Literature
1.
go back to reference Sturm D, Pfister SM, Jones DTW (2017) Pediatric gliomas: current concepts on diagnosis, biology, and clinical management. J Clin Oncol 35(21):2370–2377CrossRefPubMed Sturm D, Pfister SM, Jones DTW (2017) Pediatric gliomas: current concepts on diagnosis, biology, and clinical management. J Clin Oncol 35(21):2370–2377CrossRefPubMed
2.
go back to reference Karsy M, Guan J, Cohen AL, Jensen RL, Colman H (2017) New molecular considerations for glioma: IDH, ATRX, BRAF, TERT, H3 K27M. Curr Neurol Neurosci Rep 17(2):19CrossRefPubMed Karsy M, Guan J, Cohen AL, Jensen RL, Colman H (2017) New molecular considerations for glioma: IDH, ATRX, BRAF, TERT, H3 K27M. Curr Neurol Neurosci Rep 17(2):19CrossRefPubMed
3.
go back to reference Rao G. Intraoperative (2017) MRI and maximizing extent of resection. Neurosurg Clin N Am 28(4):477–485CrossRefPubMed Rao G. Intraoperative (2017) MRI and maximizing extent of resection. Neurosurg Clin N Am 28(4):477–485CrossRefPubMed
4.
go back to reference Lau D, Hervey-Jumper SL, Han SJ, Berger MS (2018) Intraoperative perception and estimates on extent of resection during awake glioma surgery: overcoming the learning curve. J Neurosurg 128(5):1410–1418CrossRefPubMed Lau D, Hervey-Jumper SL, Han SJ, Berger MS (2018) Intraoperative perception and estimates on extent of resection during awake glioma surgery: overcoming the learning curve. J Neurosurg 128(5):1410–1418CrossRefPubMed
5.
go back to reference Roder C, Bisdas S, Ebner FH et al (2014) 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 40(3):297–304CrossRefPubMed Roder C, Bisdas S, Ebner FH et al (2014) 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 40(3):297–304CrossRefPubMed
6.
go back to reference Roder C, Breitkopf M, Ms et al (2016) Beneficial impact of high-field intraoperative magnetic resonance imaging on the efficacy of pediatric low-grade glioma surgery. Neurosurg Focus 40(3):E13CrossRefPubMed Roder C, Breitkopf M, Ms et al (2016) Beneficial impact of high-field intraoperative magnetic resonance imaging on the efficacy of pediatric low-grade glioma surgery. Neurosurg Focus 40(3):E13CrossRefPubMed
7.
go back to reference Senft C, Bink A, Franz K et al (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12(11):997–1003CrossRefPubMed Senft C, Bink A, Franz K et al (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12(11):997–1003CrossRefPubMed
8.
go back to reference Wu JS, Gong X, Song YY et al (2014) 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 61(Suppl 1):145–154CrossRefPubMed Wu JS, Gong X, Song YY et al (2014) 3.0-T intraoperative magnetic resonance imaging-guided resection in cerebral glioma surgery: interim analysis of a prospective, randomized, triple-blind, parallel-controlled trial. Neurosurgery 61(Suppl 1):145–154CrossRefPubMed
9.
go back to reference Samdani AF, Schulder M, Catrambone JE, Carmel PW (2005) Use of a compact intraoperative low-field magnetic imager in pediatric neurosurgery. Childs Nerv Syst 21(2):108–113; discussion 114CrossRefPubMed Samdani AF, Schulder M, Catrambone JE, Carmel PW (2005) Use of a compact intraoperative low-field magnetic imager in pediatric neurosurgery. Childs Nerv Syst 21(2):108–113; discussion 114CrossRefPubMed
10.
go back to reference Shah MN, Leonard JR, Inder G et al (2012) Intraoperative magnetic resonance imaging to reduce the rate of early reoperation for lesion resection in pediatric neurosurgery. J Neurosurg Pediatr 9(3):259–264CrossRefPubMed Shah MN, Leonard JR, Inder G et al (2012) Intraoperative magnetic resonance imaging to reduce the rate of early reoperation for lesion resection in pediatric neurosurgery. J Neurosurg Pediatr 9(3):259–264CrossRefPubMed
11.
go back to reference Tejada S, Avula S, Pettorini B et al (2018) The impact of intraoperative magnetic resonance in routine pediatric neurosurgical practice-a 6-year appraisal. Childs Nerv Syst 34(4):617–626CrossRefPubMed Tejada S, Avula S, Pettorini B et al (2018) The impact of intraoperative magnetic resonance in routine pediatric neurosurgical practice-a 6-year appraisal. Childs Nerv Syst 34(4):617–626CrossRefPubMed
12.
go back to reference Kaya S, Deniz S, Duz B, Daneyemez M, Gonul E (2012) Use of an ultra-low field intraoperative MRI system for pediatric brain tumor cases: initial experience with ‘PoleStar N20’. Turk Neurosurg 22(2):218–225PubMed Kaya S, Deniz S, Duz B, Daneyemez M, Gonul E (2012) Use of an ultra-low field intraoperative MRI system for pediatric brain tumor cases: initial experience with ‘PoleStar N20’. Turk Neurosurg 22(2):218–225PubMed
13.
go back to reference Kubben PL, ter Meulen KJ, Schijns OE et al (2011) Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 12(11):1062–1070CrossRefPubMed Kubben PL, ter Meulen KJ, Schijns OE et al (2011) Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 12(11):1062–1070CrossRefPubMed
14.
go back to reference Theodosopoulos PV, Leach J, Kerr RG et al (2010) Maximizing the extent of tumor resection during transsphenoidal surgery for pituitary macroadenomas: can endoscopy replace intraoperative magnetic resonance imaging? J Neurosurg 112(4):736–743CrossRefPubMed Theodosopoulos PV, Leach J, Kerr RG et al (2010) Maximizing the extent of tumor resection during transsphenoidal surgery for pituitary macroadenomas: can endoscopy replace intraoperative magnetic resonance imaging? J Neurosurg 112(4):736–743CrossRefPubMed
15.
go back to reference Sylvester PT, Evans JA, Zipfel GJ et al (2015) Combined high-field intraoperative magnetic resonance imaging and endoscopy increase extent of resection and progression-free survival for pituitary adenomas. Pituitary 18(1):72–85CrossRefPubMedPubMedCentral Sylvester PT, Evans JA, Zipfel GJ et al (2015) Combined high-field intraoperative magnetic resonance imaging and endoscopy increase extent of resection and progression-free survival for pituitary adenomas. Pituitary 18(1):72–85CrossRefPubMedPubMedCentral
16.
go back to reference Schwartz TH, Stieg PE, Anand VK. Endoscopic transsphenoidal pituitary surgery with intraoperative magnetic resonance imaging. Neurosurgery. 2006;58(1 Suppl):ONS44-51; discussion ONS44-51. Schwartz TH, Stieg PE, Anand VK. Endoscopic transsphenoidal pituitary surgery with intraoperative magnetic resonance imaging. Neurosurgery. 2006;58(1 Suppl):ONS44-51; discussion ONS44-51.
17.
go back to reference Leuthardt EC, Lim CC, Shah MN et al (2011) Use of movable high-field-strength intraoperative magnetic resonance imaging with awake craniotomies for resection of gliomas: preliminary experience. Neurosurgery 69(1):194–205; discussion 205 – 196CrossRefPubMed Leuthardt EC, Lim CC, Shah MN et al (2011) Use of movable high-field-strength intraoperative magnetic resonance imaging with awake craniotomies for resection of gliomas: preliminary experience. Neurosurgery 69(1):194–205; discussion 205 – 196CrossRefPubMed
18.
go back to reference Giordano M, Samii A, Lawson McLean AC et al (2017) Intraoperative magnetic resonance imaging in pediatric neurosurgery: safety and utility. J Neurosurg Pediatr 19(1):77–84CrossRefPubMed Giordano M, Samii A, Lawson McLean AC et al (2017) Intraoperative magnetic resonance imaging in pediatric neurosurgery: safety and utility. J Neurosurg Pediatr 19(1):77–84CrossRefPubMed
19.
go back to reference Chen LF, Yang Y, Ma XD et al (2017) Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 27(5):696–706PubMed Chen LF, Yang Y, Ma XD et al (2017) Optimizing the extent of resection and minimizing the morbidity in insular high-grade glioma surgery by high-field intraoperative MRI guidance. Turk Neurosurg 27(5):696–706PubMed
20.
go back to reference Coburger J, Wirtz CR, Konig RW (2017) Impact of extent of resection and recurrent surgery on clinical outcome and overall survival in a consecutive series of 170 patients for glioblastoma in intraoperative high field magnetic resonance imaging. J Neurosurg Sci 61(3):233–244PubMed Coburger J, Wirtz CR, Konig RW (2017) Impact of extent of resection and recurrent surgery on clinical outcome and overall survival in a consecutive series of 170 patients for glioblastoma in intraoperative high field magnetic resonance imaging. J Neurosurg Sci 61(3):233–244PubMed
21.
go back to reference Coburger J, Merkel A, Scherer M et al (2016) 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 78(6):775–786CrossRefPubMed Coburger J, Merkel A, Scherer M et al (2016) 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 78(6):775–786CrossRefPubMed
22.
go back to reference Jenkinson MD, Barone DG, Bryant A et al (2018) Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 1:CD012788PubMed Jenkinson MD, Barone DG, Bryant A et al (2018) Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 1:CD012788PubMed
23.
go back to reference Li P, Qian R, Niu C, Fu X (2017) Impact of intraoperative MRI-guided resection on resection and survival in patient with gliomas: a meta-analysis. Curr Med Res Opin 33(4):621–630CrossRefPubMed Li P, Qian R, Niu C, Fu X (2017) Impact of intraoperative MRI-guided resection on resection and survival in patient with gliomas: a meta-analysis. Curr Med Res Opin 33(4):621–630CrossRefPubMed
24.
go back to reference Coburger J, Hagel V, Wirtz CR, Konig R (2015) Surgery for glioblastoma: impact of the combined use of 5-aminolevulinic acid and intraoperative MRI on extent of resection and survival. PLoS ONE 10(6):e0131872CrossRefPubMedPubMedCentral Coburger J, Hagel V, Wirtz CR, Konig R (2015) Surgery for glioblastoma: impact of the combined use of 5-aminolevulinic acid and intraoperative MRI on extent of resection and survival. PLoS ONE 10(6):e0131872CrossRefPubMedPubMedCentral
25.
go back to reference Quick-Weller J, Lescher S, Forster MT et al (2016) Combination of 5-ALA and iMRI in re-resection of recurrent glioblastoma. Br J Neurosurg 30(3):313–317CrossRefPubMed Quick-Weller J, Lescher S, Forster MT et al (2016) Combination of 5-ALA and iMRI in re-resection of recurrent glioblastoma. Br J Neurosurg 30(3):313–317CrossRefPubMed
26.
go back to reference Nickel K, Renovanz M, Konig J et al (2018) The patients’ view: impact of the extent of resection, intraoperative imaging, and awake surgery on health-related quality of life in high-grade glioma patients-results of a multicenter cross-sectional study. Neurosurg Rev 41(1):207–219CrossRefPubMed Nickel K, Renovanz M, Konig J et al (2018) The patients’ view: impact of the extent of resection, intraoperative imaging, and awake surgery on health-related quality of life in high-grade glioma patients-results of a multicenter cross-sectional study. Neurosurg Rev 41(1):207–219CrossRefPubMed
27.
go back to reference Coburger J, Nabavi A, Konig R, Wirtz CR, Pala A (2017) Contemporary use of intraoperative imaging in glioma surgery: a survey among EANS members. Clin Neurol Neurosurg 163:133–141CrossRefPubMed Coburger J, Nabavi A, Konig R, Wirtz CR, Pala A (2017) Contemporary use of intraoperative imaging in glioma surgery: a survey among EANS members. Clin Neurol Neurosurg 163:133–141CrossRefPubMed
28.
go back to reference Suero Molina E, Schipmann S, Stummer W. Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery-review of the literature. Neurosurg Rev 2017 Suero Molina E, Schipmann S, Stummer W. Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery-review of the literature. Neurosurg Rev 2017
29.
go back to reference Motomura K, Natsume A, Iijima K et al (2017) Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas. J Neurosurg 127(4):790–797CrossRefPubMed Motomura K, Natsume A, Iijima K et al (2017) Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas. J Neurosurg 127(4):790–797CrossRefPubMed
30.
go back to reference Lam CH, Hall WA, Truwit CL, Liu H (2001) Intra-operative MRI-guided approaches to the pediatric posterior fossa tumors. Pediatr Neurosurg 34(6):295–300CrossRefPubMed Lam CH, Hall WA, Truwit CL, Liu H (2001) Intra-operative MRI-guided approaches to the pediatric posterior fossa tumors. Pediatr Neurosurg 34(6):295–300CrossRefPubMed
31.
go back to reference Hall WA, Kowalik K, Liu H, Truwit CL, Kucharezyk J (2003) Costs and benefits of intraoperative MR-guided brain tumor resection. Acta Neurochir Suppl 85:137–142CrossRefPubMed Hall WA, Kowalik K, Liu H, Truwit CL, Kucharezyk J (2003) Costs and benefits of intraoperative MR-guided brain tumor resection. Acta Neurochir Suppl 85:137–142CrossRefPubMed
32.
go back to reference Nimsky C, Ganslandt O, Gralla J, Buchfelder M, Fahlbusch R (2003) Intraoperative low-field magnetic resonance imaging in pediatric neurosurgery. Pediatr Neurosurg 38(2):83–89CrossRefPubMed Nimsky C, Ganslandt O, Gralla J, Buchfelder M, Fahlbusch R (2003) Intraoperative low-field magnetic resonance imaging in pediatric neurosurgery. Pediatr Neurosurg 38(2):83–89CrossRefPubMed
33.
go back to reference Roth J, Beni Adani L, Biyani N, Constantini S (2006) Intraoperative portable 0.12-tesla MRI in pediatric neurosurgery. Pediatr Neurosurg 42(2):74–80CrossRefPubMed Roth J, Beni Adani L, Biyani N, Constantini S (2006) Intraoperative portable 0.12-tesla MRI in pediatric neurosurgery. Pediatr Neurosurg 42(2):74–80CrossRefPubMed
34.
go back to reference Kremer P, Tronnier V, Steiner HH et al (2006) Intraoperative MRI for interventional neurosurgical procedures and tumor resection control in children. Childs Nerv Syst 22(7):674–678CrossRefPubMed Kremer P, Tronnier V, Steiner HH et al (2006) Intraoperative MRI for interventional neurosurgical procedures and tumor resection control in children. Childs Nerv Syst 22(7):674–678CrossRefPubMed
35.
go back to reference Levy R, Cox RG, Hader WJ et al (2009) Application of intraoperative high-field magnetic resonance imaging in pediatric neurosurgery. J Neurosurg Pediatr 4(5):467–474CrossRefPubMed Levy R, Cox RG, Hader WJ et al (2009) Application of intraoperative high-field magnetic resonance imaging in pediatric neurosurgery. J Neurosurg Pediatr 4(5):467–474CrossRefPubMed
36.
go back to reference Chicoine MR, Lim CC, Evans JA et al (2011) 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 109:97–102CrossRefPubMed Chicoine MR, Lim CC, Evans JA et al (2011) 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 109:97–102CrossRefPubMed
37.
go back to reference Yousaf J, Avula S, Abernethy LJ, Mallucci CL (2012) Importance of intraoperative magnetic resonance imaging for pediatric brain tumor surgery. Surg Neurol Int 3(Suppl 2):S65–S72PubMedPubMedCentral Yousaf J, Avula S, Abernethy LJ, Mallucci CL (2012) Importance of intraoperative magnetic resonance imaging for pediatric brain tumor surgery. Surg Neurol Int 3(Suppl 2):S65–S72PubMedPubMedCentral
38.
go back to reference Kubben PL, van Santbrink H, ter Laak-Poort M et al (2012) Implementation of a mobile 0.15-T intraoperative MR system in pediatric neuro-oncological surgery: feasibility and correlation with early postoperative high-field strength MRI. Childs Nerv Syst 28(8):1171–1180CrossRefPubMedPubMedCentral Kubben PL, van Santbrink H, ter Laak-Poort M et al (2012) Implementation of a mobile 0.15-T intraoperative MR system in pediatric neuro-oncological surgery: feasibility and correlation with early postoperative high-field strength MRI. Childs Nerv Syst 28(8):1171–1180CrossRefPubMedPubMedCentral
39.
go back to reference Avula S, Pettorini B, Abernethy L et al (2013) High field strength magnetic resonance imaging in paediatric brain tumour surgery–its role in prevention of early repeat resections. Childs Nerv Syst 29(10):1843–1850CrossRefPubMed Avula S, Pettorini B, Abernethy L et al (2013) High field strength magnetic resonance imaging in paediatric brain tumour surgery–its role in prevention of early repeat resections. Childs Nerv Syst 29(10):1843–1850CrossRefPubMed
40.
go back to reference Choudhri AF, Klimo P Jr, Auschwitz TS, Whitehead MT, Boop FA (2014) 3T intraoperative MRI for management of pediatric CNS neoplasms. AJNR Am J Neuroradiol 35(12):2382–2387CrossRefPubMed Choudhri AF, Klimo P Jr, Auschwitz TS, Whitehead MT, Boop FA (2014) 3T intraoperative MRI for management of pediatric CNS neoplasms. AJNR Am J Neuroradiol 35(12):2382–2387CrossRefPubMed
Metadata
Title
Evaluation of pediatric glioma outcomes using intraoperative MRI: a multicenter cohort study
Authors
Michael Karsy
S. Hassan Akbari
David Limbrick
Eric C. Leuthardt
John Evans
Matthew D. Smyth
Jennifer Strahle
Jeffrey Leonard
Samuel Cheshier
Douglas L. Brockmeyer
Robert J. Bollo
John R. Kestle
John Honeycutt
David J. Donahue
Richard A. Roberts
Daniel R. Hansen
Jay Riva-Cambrin
Garnette Sutherland
Clair Gallagher
Walter Hader
Yves Starreveld
Mark Hamilton
Ann-Christine Duhaime
Randy L. Jensen
Michael R. Chicoine
Publication date
01-06-2019
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2019
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-019-03154-7

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