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Published in: European Radiology 6/2018

01-06-2018 | Oncology

A predictive model for distinguishing radiation necrosis from tumour progression after gamma knife radiosurgery based on radiomic features from MR images

Authors: Zijian Zhang, Jinzhong Yang, Angela Ho, Wen Jiang, Jennifer Logan, Xin Wang, Paul D. Brown, Susan L. McGovern, Nandita Guha-Thakurta, Sherise D. Ferguson, Xenia Fave, Lifei Zhang, Dennis Mackin, Laurence E. Court, Jing Li

Published in: European Radiology | Issue 6/2018

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Abstract

Objectives

To develop a model using radiomic features extracted from MR images to distinguish radiation necrosis from tumour progression in brain metastases after Gamma Knife radiosurgery.

Methods

We retrospectively identified 87 patients with pathologically confirmed necrosis (24 lesions) or progression (73 lesions) and calculated 285 radiomic features from four MR sequences (T1, T1 post-contrast, T2, and fluid-attenuated inversion recovery) obtained at two follow-up time points per lesion per patient. Reproducibility of each feature between the two time points was calculated within each group to identify a subset of features with distinct reproducible values between two groups. Changes in radiomic features from one time point to the next (delta radiomics) were used to build a model to classify necrosis and progression lesions.

Results

A combination of five radiomic features from both T1 post-contrast and T2 MR images were found to be useful in distinguishing necrosis from progression lesions. Delta radiomic features with a RUSBoost ensemble classifier had an overall predictive accuracy of 73.2% and an area under the curve value of 0.73 in leave-one-out cross-validation.

Conclusions

Delta radiomic features extracted from MR images have potential for distinguishing radiation necrosis from tumour progression after radiosurgery for brain metastases.

Key points

• Some radiomic features showed better reproducibility for progressive lesions than necrotic ones
• Delta radiomic features can help to distinguish radiation necrosis from tumour progression
• Delta radiomic features had better predictive value than did traditional radiomic features
Literature
1.
go back to reference Nayak L, Lee EQ, Wen PY (2012) Epidemiology of brain metastases. Current Oncology Reports 14:48–54CrossRefPubMed Nayak L, Lee EQ, Wen PY (2012) Epidemiology of brain metastases. Current Oncology Reports 14:48–54CrossRefPubMed
2.
go back to reference Kondziolka D, Martin JJ, Flickinger JC et al (2005) Long-term survivors after gamma knife radiosurgery for brain metastases. Cancer 104:2784–2791CrossRefPubMed Kondziolka D, Martin JJ, Flickinger JC et al (2005) Long-term survivors after gamma knife radiosurgery for brain metastases. Cancer 104:2784–2791CrossRefPubMed
3.
go back to reference Elaimy AL, Mackay AR, Lamoreaux WT et al (2011) Clinical outcomes of stereotactic radiosurgery in the treatment of patients with metastatic brain tumors. World Neurosurg 75:673–683CrossRefPubMed Elaimy AL, Mackay AR, Lamoreaux WT et al (2011) Clinical outcomes of stereotactic radiosurgery in the treatment of patients with metastatic brain tumors. World Neurosurg 75:673–683CrossRefPubMed
4.
go back to reference Minniti G, Clarke E, Lanzetta G et al (2011) Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis. Radiation Oncology 6:48CrossRefPubMedPubMedCentral Minniti G, Clarke E, Lanzetta G et al (2011) Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis. Radiation Oncology 6:48CrossRefPubMedPubMedCentral
5.
go back to reference Shaw E, Scott C, Souhami L et al (2000) Single dose radiosurgical treatment of recurrent previously irradiated primary brain tumors and brain metastases: Final report of RTOG protocol 90-05. International Journal of Radiation Oncology Biology Physics 47:291–298CrossRef Shaw E, Scott C, Souhami L et al (2000) Single dose radiosurgical treatment of recurrent previously irradiated primary brain tumors and brain metastases: Final report of RTOG protocol 90-05. International Journal of Radiation Oncology Biology Physics 47:291–298CrossRef
6.
go back to reference Chuang MT, Liu YS, Tsai YS, Chen YC, Wang CK (2016) Differentiating Radiation-Induced Necrosis from Recurrent Brain Tumor Using MR Perfusion and Spectroscopy: A Meta-Analysis. PLoS ONE 11 Chuang MT, Liu YS, Tsai YS, Chen YC, Wang CK (2016) Differentiating Radiation-Induced Necrosis from Recurrent Brain Tumor Using MR Perfusion and Spectroscopy: A Meta-Analysis. PLoS ONE 11
7.
go back to reference Lai G, Mahadevan A, Hackney D et al (2015) Diagnostic Accuracy of PET, SPECT, and Arterial Spin-Labeling in Differentiating Tumor Recurrence from Necrosis in Cerebral Metastasis after Stereotactic Radiosurgery. American Journal of Neuroradiology 36:2250–2255CrossRefPubMed Lai G, Mahadevan A, Hackney D et al (2015) Diagnostic Accuracy of PET, SPECT, and Arterial Spin-Labeling in Differentiating Tumor Recurrence from Necrosis in Cerebral Metastasis after Stereotactic Radiosurgery. American Journal of Neuroradiology 36:2250–2255CrossRefPubMed
8.
go back to reference Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nature Communications 5 Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nature Communications 5
9.
go back to reference Fehr D, Veeraraghavan H, Wibmer A et al (2015) Automatic classification of prostate cancer Gleason scores from multiparametric magnetic resonance images. Proceedings of the National Academy of Sciences 112:E6265–E6273CrossRef Fehr D, Veeraraghavan H, Wibmer A et al (2015) Automatic classification of prostate cancer Gleason scores from multiparametric magnetic resonance images. Proceedings of the National Academy of Sciences 112:E6265–E6273CrossRef
10.
go back to reference Gevaert O, Mitchell LA, Achrol AS et al (2014) Glioblastoma multiforme: exploratory radiogenomic analysis by using quantitative image features. Radiology 273:168–174CrossRefPubMedPubMedCentral Gevaert O, Mitchell LA, Achrol AS et al (2014) Glioblastoma multiforme: exploratory radiogenomic analysis by using quantitative image features. Radiology 273:168–174CrossRefPubMedPubMedCentral
12.
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. Science translational medicine 7:303ra138–303ra138CrossRefPubMedPubMedCentral Itakura H, Achrol AS, Mitchell LA et al (2015) Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities. Science translational medicine 7:303ra138–303ra138CrossRefPubMedPubMedCentral
13.
go back to reference Yamamoto S, Han W, Kim Y et al (2015) Breast cancer: radiogenomic biomarker reveals associations among dynamic contrast-enhanced MR imaging, long noncoding RNA, and metastasis. Radiology 275:384–392CrossRefPubMed Yamamoto S, Han W, Kim Y et al (2015) Breast cancer: radiogenomic biomarker reveals associations among dynamic contrast-enhanced MR imaging, long noncoding RNA, and metastasis. Radiology 275:384–392CrossRefPubMed
14.
go back to reference Mattes D, Haynor DR, Vesselle H, Lewellen TK, Eubank W (2003) PET-CT image registration in the chest using free-form deformations. IEEE Transactions On Medical Imaging 22:120–128CrossRefPubMed Mattes D, Haynor DR, Vesselle H, Lewellen TK, Eubank W (2003) PET-CT image registration in the chest using free-form deformations. IEEE Transactions On Medical Imaging 22:120–128CrossRefPubMed
15.
go back to reference Zhang L, Fried DV, Fave XJ, Hunter LA, Yang J, Court LE (2015) IBEX: An open infrastructure software platform to facilitate collaborative work in radiomics. Medical Physics 42:1341–1353CrossRefPubMedPubMedCentral Zhang L, Fried DV, Fave XJ, Hunter LA, Yang J, Court LE (2015) IBEX: An open infrastructure software platform to facilitate collaborative work in radiomics. Medical Physics 42:1341–1353CrossRefPubMedPubMedCentral
16.
go back to reference Yang J, Zhang L, Fave XJ et al (2016) Uncertainty analysis of quantitative imaging features extracted from contrast-enhanced CT in lung tumors. Comput Med Imaging Graph 48:1–8CrossRefPubMed Yang J, Zhang L, Fave XJ et al (2016) Uncertainty analysis of quantitative imaging features extracted from contrast-enhanced CT in lung tumors. Comput Med Imaging Graph 48:1–8CrossRefPubMed
17.
go back to reference Burger W, Burge MJ (2013) Edge-Preserving Smoothing FiltersPrinciples of Digital Image Processing. Springer, pp 119-167 Burger W, Burge MJ (2013) Edge-Preserving Smoothing FiltersPrinciples of Digital Image Processing. Springer, pp 119-167
18.
go back to reference Cunliffe AR, Armato Iii SG, Fei XM, Tuohy RE, Al-Hallaq HA (2013) Lung texture in serial thoracic CT scans: Registration-based methods to compare anatomically matched regionsa. Medical Physics 40:061906CrossRefPubMedPubMedCentral Cunliffe AR, Armato Iii SG, Fei XM, Tuohy RE, Al-Hallaq HA (2013) Lung texture in serial thoracic CT scans: Registration-based methods to compare anatomically matched regionsa. Medical Physics 40:061906CrossRefPubMedPubMedCentral
19.
go back to reference Fried DV, Tucker SL, Zhou S et al (2014) Prognostic value and reproducibility of pretreatment CT texture features in stage III non-small cell lung cancer. Int J Radiat Oncol Biol Phys 90:834–842CrossRefPubMedPubMedCentral Fried DV, Tucker SL, Zhou S et al (2014) Prognostic value and reproducibility of pretreatment CT texture features in stage III non-small cell lung cancer. Int J Radiat Oncol Biol Phys 90:834–842CrossRefPubMedPubMedCentral
20.
go back to reference Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE T. Syst. Man Cyb. 3:610–621CrossRef Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE T. Syst. Man Cyb. 3:610–621CrossRef
21.
go back to reference Tang X (1998) Texture information in run-length matrices. IEEE Transactions on Image Processing 7:1602–1609CrossRefPubMed Tang X (1998) Texture information in run-length matrices. IEEE Transactions on Image Processing 7:1602–1609CrossRefPubMed
22.
go back to reference Legland D, Kiêu K, Devaux M-F (2007) Computation of Minkowski measures on 2D and 3D binary images. Image Anal Stereol 26:83–92CrossRef Legland D, Kiêu K, Devaux M-F (2007) Computation of Minkowski measures on 2D and 3D binary images. Image Anal Stereol 26:83–92CrossRef
23.
go back to reference Basu S (2012) Developing predictive models for lung tumor analysis. Basu S (2012) Developing predictive models for lung tumor analysis.
24.
go back to reference Amadasun M, King R (1989) Textural Features Corresponding to Textural Properties. Ieee Transactions on Systems Man and Cybernetics 19:1264–1274CrossRef Amadasun M, King R (1989) Textural Features Corresponding to Textural Properties. Ieee Transactions on Systems Man and Cybernetics 19:1264–1274CrossRef
25.
go back to reference Dalal N, Triggs B (2005) Histograms of oriented gradients for human detection IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR) pp 886-893 Dalal N, Triggs B (2005) Histograms of oriented gradients for human detection IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR) pp 886-893
26.
go back to reference Tiwari P, Prasanna P, Wolansky L et al (2016) Computer-Extracted Texture Features to Distinguish Cerebral Radionecrosis from Recurrent Brain Tumors on Multiparametric MRI: A Feasibility Study. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A4931 Tiwari P, Prasanna P, Wolansky L et al (2016) Computer-Extracted Texture Features to Distinguish Cerebral Radionecrosis from Recurrent Brain Tumors on Multiparametric MRI: A Feasibility Study. AJNR Am J Neuroradiol. https://​doi.​org/​10.​3174/​ajnr.​A4931
27.
go back to reference Galizia MS, Töre HG, Chalian H, McCarthy R, Salem R, Yaghmai V (2012) MDCT necrosis quantification in the assessment of hepatocellular carcinoma response to yttrium 90 radioembolization therapy: comparison of two-dimensional and volumetric techniques. Academic Radiology 19:48–54CrossRefPubMed Galizia MS, Töre HG, Chalian H, McCarthy R, Salem R, Yaghmai V (2012) MDCT necrosis quantification in the assessment of hepatocellular carcinoma response to yttrium 90 radioembolization therapy: comparison of two-dimensional and volumetric techniques. Academic Radiology 19:48–54CrossRefPubMed
28.
go back to reference Lin LIK (1989) A Concordance Correlation Coefficient to Evaluate Reproducibility. Biometrics 45:255–268CrossRefPubMed Lin LIK (1989) A Concordance Correlation Coefficient to Evaluate Reproducibility. Biometrics 45:255–268CrossRefPubMed
29.
go back to reference Duda RO, Hart PE, Stork DG (2001) Pattern Classification. John Wiley and Sons, Inc. Duda RO, Hart PE, Stork DG (2001) Pattern Classification. John Wiley and Sons, Inc.
30.
go back to reference Seiffert C, Khoshgoftaar TM, Van Hulse J, Napolitano A (2010) RUSBoost: A Hybrid Approach to Alleviating Class Imbalance. Ieee Transactions on Systems Man and Cybernetics Part a-Systems and Humans 40:185-197 Seiffert C, Khoshgoftaar TM, Van Hulse J, Napolitano A (2010) RUSBoost: A Hybrid Approach to Alleviating Class Imbalance. Ieee Transactions on Systems Man and Cybernetics Part a-Systems and Humans 40:185-197
31.
go back to reference Barajas RF, Chang JS, Segal MR et al (2009) Differentiation of Recurrent Glioblastoma Multiforme from Radiation Necrosis after External Beam Radiation Therapy with Dynamic Susceptibility-weighted Contrast-enhanced Perfusion MR Imaging. Radiology 253:486–496CrossRefPubMedPubMedCentral Barajas RF, Chang JS, Segal MR et al (2009) Differentiation of Recurrent Glioblastoma Multiforme from Radiation Necrosis after External Beam Radiation Therapy with Dynamic Susceptibility-weighted Contrast-enhanced Perfusion MR Imaging. Radiology 253:486–496CrossRefPubMedPubMedCentral
32.
go back to reference Kickingereder P, Burth S, Wick A et al (2016) Radiomic Profiling of Glioblastoma: Identifying an Imaging Predictor of Patient Survival with Improved Performance over Established Clinical and Radiologic Risk Models. Radiology 280:880–889CrossRefPubMed Kickingereder P, Burth S, Wick A et al (2016) Radiomic Profiling of Glioblastoma: Identifying an Imaging Predictor of Patient Survival with Improved Performance over Established Clinical and Radiologic Risk Models. Radiology 280:880–889CrossRefPubMed
33.
go back to reference Li H, Zhu Y, Burnside ES et al (2016) MR Imaging Radiomics Signatures for Predicting the Risk of Breast Cancer Recurrence as Given by Research Versions of MammaPrint, Oncotype DX, and PAM50 Gene Assays. Radiology:152110 Li H, Zhu Y, Burnside ES et al (2016) MR Imaging Radiomics Signatures for Predicting the Risk of Breast Cancer Recurrence as Given by Research Versions of MammaPrint, Oncotype DX, and PAM50 Gene Assays. Radiology:152110
34.
go back to reference Larroza A, Moratal D, Paredes-Sánchez A et al (2015) Support vector machine classification of brain metastasis and radiation necrosis based on texture analysis in MRI. Journal of Magnetic Resonance Imaging 42:1362–1368CrossRefPubMed Larroza A, Moratal D, Paredes-Sánchez A et al (2015) Support vector machine classification of brain metastasis and radiation necrosis based on texture analysis in MRI. Journal of Magnetic Resonance Imaging 42:1362–1368CrossRefPubMed
35.
go back to reference Shinohara RT, Sweeney EM, Goldsmith J et al (2014) Statistical normalization techniques for magnetic resonance imaging. NeuroImage: Clinical 6:9–19CrossRef Shinohara RT, Sweeney EM, Goldsmith J et al (2014) Statistical normalization techniques for magnetic resonance imaging. NeuroImage: Clinical 6:9–19CrossRef
Metadata
Title
A predictive model for distinguishing radiation necrosis from tumour progression after gamma knife radiosurgery based on radiomic features from MR images
Authors
Zijian Zhang
Jinzhong Yang
Angela Ho
Wen Jiang
Jennifer Logan
Xin Wang
Paul D. Brown
Susan L. McGovern
Nandita Guha-Thakurta
Sherise D. Ferguson
Xenia Fave
Lifei Zhang
Dennis Mackin
Laurence E. Court
Jing Li
Publication date
01-06-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 6/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5154-8

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