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Published in: Acta Neurochirurgica 3/2019

01-03-2019 | Glioma | Original Article - Tumor - Glioma

Radiology reporting of low-grade glioma growth underestimates tumor expansion

Authors: Chloe Gui, Jonathan C. Lau, Suzanne E. Kosteniuk, Donald H. Lee, Joseph F. Megyesi

Published in: Acta Neurochirurgica | Issue 3/2019

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Abstract

Background

An important aspect in the management of patients with diffuse low-grade gliomas (LGGs) involves monitoring the lesions via serial magnetic resonance imaging (MRI). However, radiological interpretations of LGG interval scans are often qualitative and thus difficult to use clinically.

Methods

To contextualize these assessments, we retrospectively compared radiological interpretations of LGG growth or stability to volume change measured by manual segmentation. Tumor diameter was also measured in one, two, and three dimensions to evaluate reported methods for assessment of glioma progression, including RECIST criteria, Macdonald/RANO criteria, and mean tumor diameter/ellipsoid method.

Results

Tumors evaluated as stable by radiologists grew a median volume of 5.1 mL (11.1%) relative to the comparison scan, and those evaluated as having grown had a median volume increase of 13.3 mL (23.7%). Diameter-based measurements corresponded well but tended to overestimate gold standard segmented volumes. In addition, agreement with segmented volume measurements improved from 17.6 ± 8.0 to 4.5 ± 5.8 to 3.9 ± 3.6 mm for diameter and from 104.0 ± 96.6 to 25.3 ± 36.8 to 15.9 ± 21.3 mL for volume with radiological measurements in one, two, and three dimensions, respectively. Measurement overestimation increased with tumor size.

Conclusions

Given accumulating evidence that LGG volume and growth are prognostic factors, there is a need for objective lesion measurement. Current radiological reporting workflows fail to appreciate and communicate the true expansion of LGGs. While volumetric analysis remains the gold standard for assessment of growth, careful diametric measurements in three dimensions may be an acceptable alternative.
Literature
1.
go back to reference Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53(4):524–528CrossRefPubMed Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53(4):524–528CrossRefPubMed
2.
go back to reference Pallud J, Blonski M, Mandonnet E et al (2013) Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology 15(5):595–606CrossRefPubMedPubMedCentral Pallud J, Blonski M, Mandonnet E et al (2013) Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology 15(5):595–606CrossRefPubMedPubMedCentral
3.
go back to reference Pallud J, Taillandier L, Capelle L, Fontaine D, Peyre M, Ducray F, Duffau H, Mandonnet E (2012) Quantitative morphological magnetic resonance imaging follow-up of low-grade glioma: a plea for systematic measurement of growth rates. Neurosurgery 71(3):729–739CrossRefPubMed Pallud J, Taillandier L, Capelle L, Fontaine D, Peyre M, Ducray F, Duffau H, Mandonnet E (2012) Quantitative morphological magnetic resonance imaging follow-up of low-grade glioma: a plea for systematic measurement of growth rates. Neurosurgery 71(3):729–739CrossRefPubMed
4.
go back to reference Peyre M, Cartalat-Carel S, Meyronet D et al (2010) Prolonged response without prolonged chemotherapy: a lesson from PCV chemotherapy in low-grade gliomas. Neuro-Oncology 12(10):1078–1082CrossRefPubMedPubMedCentral Peyre M, Cartalat-Carel S, Meyronet D et al (2010) Prolonged response without prolonged chemotherapy: a lesson from PCV chemotherapy in low-grade gliomas. Neuro-Oncology 12(10):1078–1082CrossRefPubMedPubMedCentral
5.
go back to reference Rees J, Watt H, Jäger HR, Benton C, Tozer D, Tofts P, Waldman A (2009) Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 72(1):54–64CrossRefPubMed Rees J, Watt H, Jäger HR, Benton C, Tozer D, Tofts P, Waldman A (2009) Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 72(1):54–64CrossRefPubMed
6.
go back to reference Brasil Caseiras G, Ciccarelli O, Altmann DR, Benton CE, Tozer DJ, Tofts PS, Yousry TA, Rees J, Waldman AD, Jäger HR (2009) Low-grade gliomas: six-month tumor growth predicts patient outcome better than admission tumor volume, relative cerebral blood volume, and apparent diffusion coefficient. Radiology 253(2):505–512CrossRefPubMed Brasil Caseiras G, Ciccarelli O, Altmann DR, Benton CE, Tozer DJ, Tofts PS, Yousry TA, Rees J, Waldman AD, Jäger HR (2009) Low-grade gliomas: six-month tumor growth predicts patient outcome better than admission tumor volume, relative cerebral blood volume, and apparent diffusion coefficient. Radiology 253(2):505–512CrossRefPubMed
7.
go back to reference Hlaihel C, Guilloton L, Guyotat J, Streichenberger N, Honnorat J, Cotton F (2010) Predictive value of multimodality MRI using conventional, perfusion, and spectroscopy MR in anaplastic transformation of low-grade oligodendrogliomas. J Neuro-Oncol 97(1):73–80CrossRef Hlaihel C, Guilloton L, Guyotat J, Streichenberger N, Honnorat J, Cotton F (2010) Predictive value of multimodality MRI using conventional, perfusion, and spectroscopy MR in anaplastic transformation of low-grade oligodendrogliomas. J Neuro-Oncol 97(1):73–80CrossRef
8.
go back to reference Pallud J, Llitjos J-F, Dhermain F et al (2012) Dynamic imaging response following radiation therapy predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology 14(4):496–505CrossRefPubMedPubMedCentral Pallud J, Llitjos J-F, Dhermain F et al (2012) Dynamic imaging response following radiation therapy predicts long-term outcomes for diffuse low-grade gliomas. Neuro-Oncology 14(4):496–505CrossRefPubMedPubMedCentral
9.
go back to reference Pallud J, Mandonnet E, Duffau H, Kujas M, Guillevin R, Galanaud D, Taillandier L, Capelle L (2006) Prognostic value of initial magnetic resonance imaging growth rates for world health organization grade II gliomas. Ann Neurol 60(3):380–383CrossRefPubMed Pallud J, Mandonnet E, Duffau H, Kujas M, Guillevin R, Galanaud D, Taillandier L, Capelle L (2006) Prognostic value of initial magnetic resonance imaging growth rates for world health organization grade II gliomas. Ann Neurol 60(3):380–383CrossRefPubMed
10.
go back to reference Gui C, Kosteniuk SE, Lau JC, Megyesi JF (2018) Tumor growth dynamics in serially-imaged low-grade glioma patients. J Neuro-Oncol 139(1):167–175CrossRef Gui C, Kosteniuk SE, Lau JC, Megyesi JF (2018) Tumor growth dynamics in serially-imaged low-grade glioma patients. J Neuro-Oncol 139(1):167–175CrossRef
11.
go back to reference Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247CrossRef Eisenhauer EA, Therasse P, Bogaerts J et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45(2):228–247CrossRef
12.
go back to reference Macdonald DR, Cascino TL, Schold SC, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8(7):1277–1280CrossRef Macdonald DR, Cascino TL, Schold SC, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8(7):1277–1280CrossRef
13.
14.
go back to reference Van Den Bent MJ, Wefel JS, Schiff D et al (2011) Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 12(6):583–593CrossRefPubMed Van Den Bent MJ, Wefel JS, Schiff D et al (2011) Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 12(6):583–593CrossRefPubMed
15.
go back to reference Galanis E, Buckner JC, Maurer MJ, Sykora R, Castillo R, Ballman KV, Erickson BJ (2006) Validation of neuroradiologic response assessment in gliomas: measurement by RECIST, two-dimensional, computer-assisted tumor area, and computer-assisted tumor volume methods. Neuro-Oncology 8(2):156–165CrossRefPubMedPubMedCentral Galanis E, Buckner JC, Maurer MJ, Sykora R, Castillo R, Ballman KV, Erickson BJ (2006) Validation of neuroradiologic response assessment in gliomas: measurement by RECIST, two-dimensional, computer-assisted tumor area, and computer-assisted tumor volume methods. Neuro-Oncology 8(2):156–165CrossRefPubMedPubMedCentral
16.
go back to reference Kesari S, Schiff D, Drappatz J et al (2009) Phase II study of protracted daily temozolomide for low-grade gliomas in adults. Clin Cancer Res 15(1):330–337CrossRefPubMed Kesari S, Schiff D, Drappatz J et al (2009) Phase II study of protracted daily temozolomide for low-grade gliomas in adults. Clin Cancer Res 15(1):330–337CrossRefPubMed
17.
go back to reference Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31(3):1116–1128CrossRef Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31(3):1116–1128CrossRef
18.
go back to reference Martin Bland J, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 327(8476):307–310CrossRef Martin Bland J, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 327(8476):307–310CrossRef
19.
go back to reference Jakola AS, Moen KG, Solheim O, Kvistad K-A (2013) “No growth” on serial MRI scans of a low grade glioma? Acta Neurochir 155(12):2243–2244CrossRefPubMed Jakola AS, Moen KG, Solheim O, Kvistad K-A (2013) “No growth” on serial MRI scans of a low grade glioma? Acta Neurochir 155(12):2243–2244CrossRefPubMed
20.
go back to reference Suzuki C, Jacobsson H, Hatschek T, Torkzad MR, Bodén K, Eriksson-Alm Y, Berg E, Fujii H, Kubo A, Blomqvist L (2008) Radiologic measurements of tumor response to treatment: practical approaches and limitations. RadioGraphics 28(2):329–344CrossRefPubMed Suzuki C, Jacobsson H, Hatschek T, Torkzad MR, Bodén K, Eriksson-Alm Y, Berg E, Fujii H, Kubo A, Blomqvist L (2008) Radiologic measurements of tumor response to treatment: practical approaches and limitations. RadioGraphics 28(2):329–344CrossRefPubMed
21.
go back to reference Dempsey MF, Condon BR, Hadley DM (2005) Measurement of tumor “size” in recurrent malignant glioma: 1D, 2D, or 3D? AJNR Am J Neuroradiol 26(4):770–776 Dempsey MF, Condon BR, Hadley DM (2005) Measurement of tumor “size” in recurrent malignant glioma: 1D, 2D, or 3D? AJNR Am J Neuroradiol 26(4):770–776
22.
go back to reference Provenzale JM, Ison C, DeLong D (2009) Bidimensional measurements in brain tumors: assessment of interobserver variability. Am J Roentgenol 193(6):515–522CrossRef Provenzale JM, Ison C, DeLong D (2009) Bidimensional measurements in brain tumors: assessment of interobserver variability. Am J Roentgenol 193(6):515–522CrossRef
23.
go back to reference Sorensen AG, Patel S, Harmath C et al (2001) Comparison of diameter and perimeter methods for tumor volume calculation. J Clin Oncol 19(2):551–557CrossRefPubMed Sorensen AG, Patel S, Harmath C et al (2001) Comparison of diameter and perimeter methods for tumor volume calculation. J Clin Oncol 19(2):551–557CrossRefPubMed
24.
go back to reference Shah GD, Kesari S, Xu R, Batchelor TT, O’Neill AM, Hochberg FH, Levy B, Bradshaw J, Wen PY (2006) Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas. Neuro-Oncology 8(1):38–46CrossRefPubMedPubMedCentral Shah GD, Kesari S, Xu R, Batchelor TT, O’Neill AM, Hochberg FH, Levy B, Bradshaw J, Wen PY (2006) Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas. Neuro-Oncology 8(1):38–46CrossRefPubMedPubMedCentral
25.
go back to reference Schmitt P, Mandonnet E, Perdreau A, Angelini ED (2013) Effects of slice thickness and head rotation when measuring glioma sizes on MRI: in support of volume segmentation versus two largest diameters methods. J Neuro-Oncol 112(2):165–172CrossRef Schmitt P, Mandonnet E, Perdreau A, Angelini ED (2013) Effects of slice thickness and head rotation when measuring glioma sizes on MRI: in support of volume segmentation versus two largest diameters methods. J Neuro-Oncol 112(2):165–172CrossRef
Metadata
Title
Radiology reporting of low-grade glioma growth underestimates tumor expansion
Authors
Chloe Gui
Jonathan C. Lau
Suzanne E. Kosteniuk
Donald H. Lee
Joseph F. Megyesi
Publication date
01-03-2019
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 3/2019
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-018-03783-3

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