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Published in: European Radiology 9/2019

Open Access 01-09-2019 | Glioblastoma | Oncology

Multi-parametric and multi-regional histogram analysis of MRI: modality integration reveals imaging phenotypes of glioblastoma

Authors: Chao Li, Shuo Wang, Angela Serra, Turid Torheim, Jiun-Lin Yan, Natalie R. Boonzaier, Yuan Huang, Tomasz Matys, Mary A. McLean, Florian Markowetz, Stephen J. Price

Published in: European Radiology | Issue 9/2019

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Abstract

Objectives

Integrating multiple imaging modalities is crucial for MRI data interpretation. The purpose of this study is to determine whether a previously proposed multi-view approach can effectively integrate the histogram features from multi-parametric MRI and whether the selected features can offer incremental prognostic values over clinical variables.

Methods

Eighty newly-diagnosed glioblastoma patients underwent surgery and chemoradiotherapy. Histogram features of diffusion and perfusion imaging were extracted from contrast-enhancing (CE) and non-enhancing (NE) regions independently. An unsupervised patient clustering was performed by the multi-view approach. Kaplan-Meier and Cox proportional hazards regression analyses were performed to evaluate the relevance of patient clustering to survival. The metabolic signatures of patient clusters were compared using multi-voxel spectroscopy analysis. The prognostic values of histogram features were evaluated by survival and ROC curve analyses.

Results

Two patient clusters were generated, consisting of 53 and 27 patients respectively. Cluster 2 demonstrated better overall survival (OS) (p = 0.007) and progression-free survival (PFS) (p < 0.001) than Cluster 1. Cluster 2 displayed lower N-acetylaspartate/creatine ratio in NE region (p = 0.040). A higher mean value of anisotropic diffusion in NE region was associated with worse OS (hazard ratio [HR] = 1.40, p = 0.020) and PFS (HR = 1.36, p = 0.031). The seven features selected by this approach showed significantly incremental value in predicting 12-month OS (p = 0.020) and PFS (p = 0.022).

Conclusions

The multi-view clustering method can provide an effective integration of multi-parametric MRI. The histogram features selected may be used as potential prognostic markers.

Key Points

• Multi-parametric magnetic resonance imaging captures multi-faceted tumor physiology.
• Contrast-enhancing and non-enhancing tumor regions represent different tumor components with distinct clinical relevance.
• Multi-view data analysis offers a method which can effectively select and integrate multi-parametric and multi-regional imaging features.
Appendix
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Literature
1.
go back to reference Ricard D, Idbaih A, Ducray F, Lahutte M, Hoang-Xuan K, Delattre JY (2012) Primary brain tumours in adults. Lancet 379:1984–1996CrossRefPubMed Ricard D, Idbaih A, Ducray F, Lahutte M, Hoang-Xuan K, Delattre JY (2012) Primary brain tumours in adults. Lancet 379:1984–1996CrossRefPubMed
2.
go back to reference Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972CrossRefPubMed Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972CrossRefPubMed
3.
go back to reference O'Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A (2015) Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 21:249–257CrossRefPubMed O'Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A (2015) Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 21:249–257CrossRefPubMed
4.
go back to reference Lupo JM, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility-weighted perfusion imaging of high-grade gliomas: characterization of spatial heterogeneity. AJNR Am J Neuroradiol 26:1446–1454PubMedPubMedCentral Lupo JM, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility-weighted perfusion imaging of high-grade gliomas: characterization of spatial heterogeneity. AJNR Am J Neuroradiol 26:1446–1454PubMedPubMedCentral
5.
go back to reference Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25:356–369PubMedPubMedCentral Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25:356–369PubMedPubMedCentral
6.
go back to reference Peña A, Green HA, Carpenter TA, Price SJ, Pickard JD, Gillard JH (2006) Enhanced visualization and quantification of magnetic resonance diffusion tensor imaging using the p:q tensor decomposition. Br J Radiol 79:101–109CrossRefPubMed Peña A, Green HA, Carpenter TA, Price SJ, Pickard JD, Gillard JH (2006) Enhanced visualization and quantification of magnetic resonance diffusion tensor imaging using the p:q tensor decomposition. Br J Radiol 79:101–109CrossRefPubMed
7.
go back to reference Price SJ, Jena R, Burnet NG, Carpenter TA, Pickard JD, Gillard JH (2007) Predicting patterns of glioma recurrence using diffusion tensor imaging. Eur Radiol 17:1675–1684CrossRefPubMed Price SJ, Jena R, Burnet NG, Carpenter TA, Pickard JD, Gillard JH (2007) Predicting patterns of glioma recurrence using diffusion tensor imaging. Eur Radiol 17:1675–1684CrossRefPubMed
8.
go back to reference Mohsen LA, Shi V, Jena R, Gillard JH, Price SJ (2013) Diffusion tensor invasive phenotypes can predict progression-free survival in glioblastomas. Br J Neurosurg 27:436–441CrossRefPubMed Mohsen LA, Shi V, Jena R, Gillard JH, Price SJ (2013) Diffusion tensor invasive phenotypes can predict progression-free survival in glioblastomas. Br J Neurosurg 27:436–441CrossRefPubMed
9.
go back to reference Howe FA, Barton SJ, Cudlip SA et al (2003) Metabolic profiles of human brain tumors using quantitative in vivo H-1 magnetic resonance spectroscopy. Magn Reson Med 49:223–232CrossRefPubMed Howe FA, Barton SJ, Cudlip SA et al (2003) Metabolic profiles of human brain tumors using quantitative in vivo H-1 magnetic resonance spectroscopy. Magn Reson Med 49:223–232CrossRefPubMed
10.
go back to reference Padhani AR, Miles KA (2010) Multiparametric imaging of tumor response to therapy. Radiology 256:348–364CrossRefPubMed Padhani AR, Miles KA (2010) Multiparametric imaging of tumor response to therapy. Radiology 256:348–364CrossRefPubMed
13.
go back to reference Fratello M, Caiazzo G, Trojsi F et al (2017) Multi-view ensemble classification of brain connectivity images for neurodegeneration type discrimination. Neuroinformatics 15:199–213CrossRefPubMedPubMedCentral Fratello M, Caiazzo G, Trojsi F et al (2017) Multi-view ensemble classification of brain connectivity images for neurodegeneration type discrimination. Neuroinformatics 15:199–213CrossRefPubMedPubMedCentral
15.
go back to reference Vogelbaum MA, Jost S, Aghi MK et al (2012) Application of novel response/progression measures for surgically delivered therapies for gliomas: response assessment in neuro-oncology (RANO) working group. Neurosurgery 70:234–243CrossRefPubMed Vogelbaum MA, Jost S, Aghi MK et al (2012) Application of novel response/progression measures for surgically delivered therapies for gliomas: response assessment in neuro-oncology (RANO) working group. Neurosurgery 70:234–243CrossRefPubMed
16.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefPubMed Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefPubMed
17.
go back to reference Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219CrossRefPubMed Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219CrossRefPubMed
18.
go back to reference Behrens TE, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088CrossRefPubMed Behrens TE, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088CrossRefPubMed
19.
go back to reference Fedorov A, Beichel R, Kalpathy-Cramer J et al (2012) 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 30:1323–1341CrossRefPubMedPubMedCentral Fedorov A, Beichel R, Kalpathy-Cramer J et al (2012) 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging 30:1323–1341CrossRefPubMedPubMedCentral
21.
go back to reference Pavlidis P, Weston J, Cai J, Grundy WN (2001) Gene functional classification from heterogeneous data. Proceedings of the fifth annual international conference on computational biology. ACM, Montreal, Quebec, Canada, pp 249–255 Pavlidis P, Weston J, Cai J, Grundy WN (2001) Gene functional classification from heterogeneous data. Proceedings of the fifth annual international conference on computational biology. ACM, Montreal, Quebec, Canada, pp 249–255
22.
go back to reference Price SJ, Young AM, Scotton WJ et al (2016) Multimodal MRI can identify perfusion and metabolic changes in the invasive margin of glioblastomas. J Magn Reson Imaging 43:487–494CrossRefPubMed Price SJ, Young AM, Scotton WJ et al (2016) Multimodal MRI can identify perfusion and metabolic changes in the invasive margin of glioblastomas. J Magn Reson Imaging 43:487–494CrossRefPubMed
23.
go back to reference Kuhn M (2008) Building predictive models in R using the caret package. J Stat Softw 28:1–26CrossRef Kuhn M (2008) Building predictive models in R using the caret package. J Stat Softw 28:1–26CrossRef
24.
go back to reference Choi YS, Ahn SS, Kim DW et al (2016) Incremental prognostic value of ADC histogram analysis over MGMT promoter methylation status in patients with glioblastoma. Radiology 281:175–184CrossRefPubMed Choi YS, Ahn SS, Kim DW et al (2016) Incremental prognostic value of ADC histogram analysis over MGMT promoter methylation status in patients with glioblastoma. Radiology 281:175–184CrossRefPubMed
25.
go back to reference Jakab A, Molnár P, Emri M, Berényi E (2011) Glioma grade assessment by using histogram analysis of diffusion tensor imaging-derived maps. Neuroradiology 53:483–491 Jakab A, Molnár P, Emri M, Berényi E (2011) Glioma grade assessment by using histogram analysis of diffusion tensor imaging-derived maps. Neuroradiology 53:483–491
26.
go back to reference Santarosa C, Castellano A, Conte GM et al (2016) Dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging for glioma grading: preliminary comparison of vessel compartment and permeability parameters using hotspot and histogram analysis. Eur J Radiol 85:1147–1156CrossRefPubMed Santarosa C, Castellano A, Conte GM et al (2016) Dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging for glioma grading: preliminary comparison of vessel compartment and permeability parameters using hotspot and histogram analysis. Eur J Radiol 85:1147–1156CrossRefPubMed
27.
go back to reference Burth S, Kickingereder P, Eidel O et al (2016) Clinical parameters outweigh diffusion- and perfusion-derived Mri parameters in predicting survival in newly-diagnosed glioblastoma. Neuro Oncol 18:34–34 Burth S, Kickingereder P, Eidel O et al (2016) Clinical parameters outweigh diffusion- and perfusion-derived Mri parameters in predicting survival in newly-diagnosed glioblastoma. Neuro Oncol 18:34–34
28.
go back to reference Çoban G, Mohan S, Kural F, Wang S, O’Rourke DM, Poptani H (2015) Prognostic value of dynamic susceptibility contrast-enhanced and diffusion-weighted MR imaging in patients with glioblastomas. AJNR Am J Neuroradiol 36:1247–1252CrossRefPubMedPubMedCentral Çoban G, Mohan S, Kural F, Wang S, O’Rourke DM, Poptani H (2015) Prognostic value of dynamic susceptibility contrast-enhanced and diffusion-weighted MR imaging in patients with glioblastomas. AJNR Am J Neuroradiol 36:1247–1252CrossRefPubMedPubMedCentral
29.
go back to reference Hilario A, Sepulveda JM, Perez-Nuñez A et al (2014) A prognostic model based on preoperative MRI predicts overall survival in patients with diffuse gliomas. AJNR Am J Neuroradiol 35:1096–1102CrossRefPubMedPubMedCentral Hilario A, Sepulveda JM, Perez-Nuñez A et al (2014) A prognostic model based on preoperative MRI predicts overall survival in patients with diffuse gliomas. AJNR Am J Neuroradiol 35:1096–1102CrossRefPubMedPubMedCentral
30.
go back to reference Grossman R, Shimony N, Shir D et al (2017) Dynamics of FLAIR volume changes in glioblastoma and prediction of survival. Ann Surg Oncol 24:794–800CrossRefPubMed Grossman R, Shimony N, Shir D et al (2017) Dynamics of FLAIR volume changes in glioblastoma and prediction of survival. Ann Surg Oncol 24:794–800CrossRefPubMed
31.
go back to reference Garrett MD, Yanagihara TK, Yeh R et al (2017) Monitoring radiation treatment effects in glioblastoma: FLAIR volume as significant predictor of survival. Tomography 3:131–137CrossRefPubMedPubMedCentral Garrett MD, Yanagihara TK, Yeh R et al (2017) Monitoring radiation treatment effects in glioblastoma: FLAIR volume as significant predictor of survival. Tomography 3:131–137CrossRefPubMedPubMedCentral
32.
go back to reference Boxerman JL, Zhang Z, Safriel Y et al (2018) Prognostic value of contrast enhancement and FLAIR for survival in newly diagnosed glioblastoma treated with and without bevacizumab: results from ACRIN 6686. Neuro Oncol 20:1400–1410CrossRefPubMedPubMedCentral Boxerman JL, Zhang Z, Safriel Y et al (2018) Prognostic value of contrast enhancement and FLAIR for survival in newly diagnosed glioblastoma treated with and without bevacizumab: results from ACRIN 6686. Neuro Oncol 20:1400–1410CrossRefPubMedPubMedCentral
33.
go back to reference Price SJ, Jena R, Burnet NG et al (2006) Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27:1969–1974PubMedPubMedCentral Price SJ, Jena R, Burnet NG et al (2006) Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27:1969–1974PubMedPubMedCentral
34.
go back to reference Yan JL, van der Hoorn A, Larkin TJ, Boonzaier NR, Matys T, Price SJ (2017) Extent of resection of peritumoral diffusion tensor imaging-detected abnormality as a predictor of survival in adult glioblastoma patients. J Neurosurg 126:234–241CrossRefPubMed Yan JL, van der Hoorn A, Larkin TJ, Boonzaier NR, Matys T, Price SJ (2017) Extent of resection of peritumoral diffusion tensor imaging-detected abnormality as a predictor of survival in adult glioblastoma patients. J Neurosurg 126:234–241CrossRefPubMed
35.
go back to reference Itakura H, Achrol AS, Mitchell LA et al (2015) Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities. Sci Transl Med 7:303ra138CrossRefPubMedPubMedCentral Itakura H, Achrol AS, Mitchell LA et al (2015) Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities. Sci Transl Med 7:303ra138CrossRefPubMedPubMedCentral
38.
go back to reference Zhou M, Scott J, Chaudhury B et al (2018) Radiomics in brain tumor: image assessment, quantitative feature descriptors, and machine-learning approaches. AJNR Am J Neuroradiol 39:208–216CrossRefPubMedPubMedCentral Zhou M, Scott J, Chaudhury B et al (2018) Radiomics in brain tumor: image assessment, quantitative feature descriptors, and machine-learning approaches. AJNR Am J Neuroradiol 39:208–216CrossRefPubMedPubMedCentral
39.
go back to reference Larue RTHM, Defraene G, De Ruysscher D, Lambin P, van Elmpt W (2017) Quantitative radiomics studies for tissue characterization: a review of technology and methodological procedures. Br J Radiol 90:20160665CrossRefPubMedPubMedCentral Larue RTHM, Defraene G, De Ruysscher D, Lambin P, van Elmpt W (2017) Quantitative radiomics studies for tissue characterization: a review of technology and methodological procedures. Br J Radiol 90:20160665CrossRefPubMedPubMedCentral
Metadata
Title
Multi-parametric and multi-regional histogram analysis of MRI: modality integration reveals imaging phenotypes of glioblastoma
Authors
Chao Li
Shuo Wang
Angela Serra
Turid Torheim
Jiun-Lin Yan
Natalie R. Boonzaier
Yuan Huang
Tomasz Matys
Mary A. McLean
Florian Markowetz
Stephen J. Price
Publication date
01-09-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 9/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5984-z

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