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Published in: European Radiology 11/2018

01-11-2018 | Magnetic Resonance

Classifying brain metastases by their primary site of origin using a radiomics approach based on texture analysis: a feasibility study

Authors: Rafael Ortiz-Ramón, Andrés Larroza, Silvia Ruiz-España, Estanislao Arana, David Moratal

Published in: European Radiology | Issue 11/2018

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Abstract

Objective

To examine the capability of MRI texture analysis to differentiate the primary site of origin of brain metastases following a radiomics approach.

Methods

Sixty-seven untreated brain metastases (BM) were found in 3D T1-weighted MRI of 38 patients with cancer: 27 from lung cancer, 23 from melanoma and 17 from breast cancer. These lesions were segmented in 2D and 3D to compare the discriminative power of 2D and 3D texture features. The images were quantized using different number of gray-levels to test the influence of quantization. Forty-three rotation-invariant texture features were examined. Feature selection and random forest classification were implemented within a nested cross-validation structure. Classification was evaluated with the area under receiver operating characteristic curve (AUC) considering two strategies: multiclass and one-versus-one.

Results

In the multiclass approach, 3D texture features were more discriminative than 2D features. The best results were achieved for images quantized with 32 gray-levels (AUC = 0.873 ± 0.064) using the top four features provided by the feature selection method based on the p-value. In the one-versus-one approach, high accuracy was obtained when differentiating lung cancer BM from breast cancer BM (four features, AUC = 0.963 ± 0.054) and melanoma BM (eight features, AUC = 0.936 ± 0.070) using the optimal dataset (3D features, 32 gray-levels). Classification of breast cancer and melanoma BM was unsatisfactory (AUC = 0.607 ± 0.180).

Conclusion

Volumetric MRI texture features can be useful to differentiate brain metastases from different primary cancers after quantizing the images with the proper number of gray-levels.

Key Points

• Texture analysis is a promising source of biomarkers for classifying brain neoplasms.
• MRI texture features of brain metastases could help identifying the primary cancer.
• Volumetric texture features are more discriminative than traditional 2D texture features.
Appendix
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Literature
1.
go back to reference Gavrilovic IT, Posner JB (2005) Brain metastases: epidemiology and pathophysiology. J Neurooncol 75:5–14CrossRef Gavrilovic IT, Posner JB (2005) Brain metastases: epidemiology and pathophysiology. J Neurooncol 75:5–14CrossRef
2.
go back to reference Stelzer KJ (2013) Epidemiology and prognosis of brain metastases. Surg Neurol Int 4:S192–S202CrossRef Stelzer KJ (2013) Epidemiology and prognosis of brain metastases. Surg Neurol Int 4:S192–S202CrossRef
3.
go back to reference Soffietti R, Cornu P, Delattre JY et al (2006) EFNS Guidelines on diagnosis and treatment of brain metastases: report of an EFNS Task Force. Eur J Neurol 13:674–681CrossRef Soffietti R, Cornu P, Delattre JY et al (2006) EFNS Guidelines on diagnosis and treatment of brain metastases: report of an EFNS Task Force. Eur J Neurol 13:674–681CrossRef
4.
go back to reference Kaal ECA, Taphoorn MJB, Vecht CJ (2005) Symptomatic management and imaging of brain metastases. J Neurooncol 75:15–20CrossRef Kaal ECA, Taphoorn MJB, Vecht CJ (2005) Symptomatic management and imaging of brain metastases. J Neurooncol 75:15–20CrossRef
5.
go back to reference Nayak L, Lee EQ, Wen PY (2012) Epidemiology of brain metastases. Curr Oncol Rep 14:48–54CrossRef Nayak L, Lee EQ, Wen PY (2012) Epidemiology of brain metastases. Curr Oncol Rep 14:48–54CrossRef
6.
go back to reference Bartelt S, Lutterbach J (2003) Brain metastases in patients with cancer of unknown primary. J Neurooncol 64:249–253CrossRef Bartelt S, Lutterbach J (2003) Brain metastases in patients with cancer of unknown primary. J Neurooncol 64:249–253CrossRef
7.
go back to reference Agazzi S, Pampallona S, Pica A et al (2004) The origin of brain metastases in patients with an undiagnosed primary tumor. Acta Neurochir (Wien) 146:153–157CrossRef Agazzi S, Pampallona S, Pica A et al (2004) The origin of brain metastases in patients with an undiagnosed primary tumor. Acta Neurochir (Wien) 146:153–157CrossRef
8.
go back to reference Pekmezci M, Perry A (2013) Neuropathology of brain metastases. Surg Neurol Int 4:245CrossRef Pekmezci M, Perry A (2013) Neuropathology of brain metastases. Surg Neurol Int 4:245CrossRef
9.
go back to reference Zakaria R, Das K, Bhojak M et al (2014) The role of magnetic resonance imaging in the management of brain metastases: diagnosis to prognosis. Cancer Imaging 14:1–8 Zakaria R, Das K, Bhojak M et al (2014) The role of magnetic resonance imaging in the management of brain metastases: diagnosis to prognosis. Cancer Imaging 14:1–8
10.
go back to reference Bekaert L, Emery E, Levallet G, Lechapt-Zalcman E (2017) Histopathologic diagnosis of brain metastases: current trends in management and future considerations. Brain Tumor Pathol 34:8–19CrossRef Bekaert L, Emery E, Levallet G, Lechapt-Zalcman E (2017) Histopathologic diagnosis of brain metastases: current trends in management and future considerations. Brain Tumor Pathol 34:8–19CrossRef
11.
go back to reference Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: images are more than pictures, they are data. Radiology 278:563–577CrossRef Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: images are more than pictures, they are data. Radiology 278:563–577CrossRef
12.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRef Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRef
13.
go back to reference Yip SSF, Aerts HJWL (2016) Applications and limitations of radiomics. Phys Med Biol 61:R150–R166CrossRef Yip SSF, Aerts HJWL (2016) Applications and limitations of radiomics. Phys Med Biol 61:R150–R166CrossRef
14.
go back to reference Kumar V, Gu Y, Basu S et al (2012) Radiomics: the process and the challenges. Magn Reson Imaging 30:1234–1248CrossRef Kumar V, Gu Y, Basu S et al (2012) Radiomics: the process and the challenges. Magn Reson Imaging 30:1234–1248CrossRef
15.
go back to reference Castellano G, Bonilha L, Li LM, Cendes F (2004) Texture analysis of medical images. Clin Radiol 59:1061–1069CrossRef Castellano G, Bonilha L, Li LM, Cendes F (2004) Texture analysis of medical images. Clin Radiol 59:1061–1069CrossRef
16.
go back to reference Kassner A, Thornhill RE (2010) Texture analysis: a review of neurologic MR imaging applications. AJNR Am J Neuroradiol 31:809–816CrossRef Kassner A, Thornhill RE (2010) Texture analysis: a review of neurologic MR imaging applications. AJNR Am J Neuroradiol 31:809–816CrossRef
17.
go back to reference Mahmoud-Ghoneim D, Toussaint G, Constans JM, De Certaines JD (2003) Three dimensional texture analysis in MRI: a preliminary evaluation in gliomas. Magn Reson Imaging 21:983–987CrossRef Mahmoud-Ghoneim D, Toussaint G, Constans JM, De Certaines JD (2003) Three dimensional texture analysis in MRI: a preliminary evaluation in gliomas. Magn Reson Imaging 21:983–987CrossRef
18.
go back to reference Fetit AE, Novak J, Peet AC, Arvanitis TN (2015) Three-dimensional textural features of conventional MRI improve diagnostic classification of childhood brain tumors. NMR Biomed 28:1174–1184CrossRef Fetit AE, Novak J, Peet AC, Arvanitis TN (2015) Three-dimensional textural features of conventional MRI improve diagnostic classification of childhood brain tumors. NMR Biomed 28:1174–1184CrossRef
19.
go back to reference Zacharaki EI, Wang S, Chawla S et al (2009) Classification of brain tumor type and grade using MRI texture and shape in a machine learning scheme. Magn Reson Med 62:1609–1618CrossRef Zacharaki EI, Wang S, Chawla S et al (2009) Classification of brain tumor type and grade using MRI texture and shape in a machine learning scheme. Magn Reson Med 62:1609–1618CrossRef
20.
go back to reference Georgiadis P, Cavouras D, Kalatzis I et al (2009) Enhancing the discrimination accuracy between metastases, gliomas and meningiomas on brain MRI by volumetric textural features and ensemble pattern recognition methods. Magn Reson Imaging 27:120–130CrossRef Georgiadis P, Cavouras D, Kalatzis I et al (2009) Enhancing the discrimination accuracy between metastases, gliomas and meningiomas on brain MRI by volumetric textural features and ensemble pattern recognition methods. Magn Reson Imaging 27:120–130CrossRef
21.
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. J Magn Reson Imaging 42:1362–1368CrossRef 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. J Magn Reson Imaging 42:1362–1368CrossRef
22.
go back to reference Li Z, Mao Y, Li H et al (2016) Differentiating brain metastases from different pathological types of lung cancers using texture analysis of T1 postcontrast MR. Magn Reson Med 76:1410–1419CrossRef Li Z, Mao Y, Li H et al (2016) Differentiating brain metastases from different pathological types of lung cancers using texture analysis of T1 postcontrast MR. Magn Reson Med 76:1410–1419CrossRef
23.
go back to reference Fink KR, Fink JR (2013) Imaging of brain metastases. Surg Neurol Int 4:S209–S219CrossRef Fink KR, Fink JR (2013) Imaging of brain metastases. Surg Neurol Int 4:S209–S219CrossRef
24.
go back to reference Larroza A, Bodí V, Moratal D (2016) Texture analysis in magnetic resonance imaging: review and considerations for future applications. In: Assessment of cellular and organ function and dysfunction using direct and derived MRI methodologies. InTech, Rijeka, Croatia, pp 75–106 Larroza A, Bodí V, Moratal D (2016) Texture analysis in magnetic resonance imaging: review and considerations for future applications. In: Assessment of cellular and organ function and dysfunction using direct and derived MRI methodologies. InTech, Rijeka, Croatia, pp 75–106
25.
go back to reference Leite M, Rittner L, Appenzeller S et al (2015) Etiology-based classification of brain white matter hyperintensity on magnetic resonance imaging. J Med Imaging 2:14002CrossRef Leite M, Rittner L, Appenzeller S et al (2015) Etiology-based classification of brain white matter hyperintensity on magnetic resonance imaging. J Med Imaging 2:14002CrossRef
26.
go back to reference Mahmoud-Ghoneim D, Alkaabi MK, De Certaines JD, Goettsche F-M (2008) The impact of image dynamic range on texture classification of brain white matter. BMC Med Imaging 8:1–8CrossRef Mahmoud-Ghoneim D, Alkaabi MK, De Certaines JD, Goettsche F-M (2008) The impact of image dynamic range on texture classification of brain white matter. BMC Med Imaging 8:1–8CrossRef
27.
go back to reference Depeursinge A, Foncubierta-Rodriguez A, Van De Ville D, Müller H (2014) Three-dimensional solid texture analysis in biomedical imaging: review and opportunities. Med Image Anal 18:176–196CrossRef Depeursinge A, Foncubierta-Rodriguez A, Van De Ville D, Müller H (2014) Three-dimensional solid texture analysis in biomedical imaging: review and opportunities. Med Image Anal 18:176–196CrossRef
28.
go back to reference Ellingson BM, Bendszus M, Boxerman J et al (2015) Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials. Neuro Oncol 17:1188–1198CrossRef Ellingson BM, Bendszus M, Boxerman J et al (2015) Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials. Neuro Oncol 17:1188–1198CrossRef
29.
go back to reference Mayerhoefer ME, Breitenseher MJ, Kramer J et al (2005) Texture analysis for tissue discrimination on T1-weighted MR images of the knee joint in a multicenter study: Transferability of texture features and comparison of feature selection methods and classifiers. J Magn Reson Imaging 22:674–680CrossRef Mayerhoefer ME, Breitenseher MJ, Kramer J et al (2005) Texture analysis for tissue discrimination on T1-weighted MR images of the knee joint in a multicenter study: Transferability of texture features and comparison of feature selection methods and classifiers. J Magn Reson Imaging 22:674–680CrossRef
30.
go back to reference Waugh SA, Lerski RA, Bidaut L, Thompson AM (2011) The influence of field strength and different clinical breast MRI protocols on the outcome of texture analysis using foam phantoms. Med Phys 38:5058–5066CrossRef Waugh SA, Lerski RA, Bidaut L, Thompson AM (2011) The influence of field strength and different clinical breast MRI protocols on the outcome of texture analysis using foam phantoms. Med Phys 38:5058–5066CrossRef
31.
go back to reference Chan TF, Vese LA (2001) Active contours without edges. IEEE Trans Image Process 10:266–277CrossRef Chan TF, Vese LA (2001) Active contours without edges. IEEE Trans Image Process 10:266–277CrossRef
32.
go back to reference Collewet G, Strzelecki M, Mariette F (2004) Influence of MRI acquisition protocols and image intensity normalization methods on texture classification. Magn Reson Imaging 22:81–91CrossRef Collewet G, Strzelecki M, Mariette F (2004) Influence of MRI acquisition protocols and image intensity normalization methods on texture classification. Magn Reson Imaging 22:81–91CrossRef
33.
go back to reference Gibbs P, Turnbull LW (2003) Textural analysis of contrast-enhanced MR images of the breast. Magn Reson Med 50:92–98CrossRef Gibbs P, Turnbull LW (2003) Textural analysis of contrast-enhanced MR images of the breast. Magn Reson Med 50:92–98CrossRef
34.
go back to reference Vallières M, Freeman CR, Skamene SR, El Naqa I (2015) A radiomics model from joint FDG-PET and MRI texture features for the prediction of lung metastases in soft-tissue sarcomas of the extremities. Phys Med Biol 60:5471–5496CrossRef Vallières M, Freeman CR, Skamene SR, El Naqa I (2015) A radiomics model from joint FDG-PET and MRI texture features for the prediction of lung metastases in soft-tissue sarcomas of the extremities. Phys Med Biol 60:5471–5496CrossRef
35.
go back to reference Kuhn M, Johnson K (2013) Data pre-processing. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 27–59CrossRef Kuhn M, Johnson K (2013) Data pre-processing. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 27–59CrossRef
36.
go back to reference Fernández-Delgado M, Cernadas E, Barro S et al (2014) Do we need hundreds of classifiers to solve real world classification problems? J Mach Learn Res 15:3133–3181 Fernández-Delgado M, Cernadas E, Barro S et al (2014) Do we need hundreds of classifiers to solve real world classification problems? J Mach Learn Res 15:3133–3181
37.
go back to reference Caruana R, Karampatziakis N, Yessenalina A (2008) An empirical evaluation of supervised learning in high dimensions. In: Proceedings of the 25th international conference on Machine learning - ICML ’08. ACM Press, Helsinki, Finland, pp 96–103 Caruana R, Karampatziakis N, Yessenalina A (2008) An empirical evaluation of supervised learning in high dimensions. In: Proceedings of the 25th international conference on Machine learning - ICML ’08. ACM Press, Helsinki, Finland, pp 96–103
38.
go back to reference Kuhn M, Johnson K (2013) Over-fitting and model tuning. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 61–92CrossRef Kuhn M, Johnson K (2013) Over-fitting and model tuning. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 61–92CrossRef
39.
go back to reference Kuhn M, Johnson K (2013) An introduction to feature selection. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 487–519CrossRef Kuhn M, Johnson K (2013) An introduction to feature selection. In: Applied predictive modeling, 1st ed. Springer, New York, NY, pp 487–519CrossRef
40.
go back to reference Ambroise C, McLachlan GJ (2002) Selection bias in gene extraction on the basis of microarray gene-expression data. Proc Natl Acad Sci U S A 99:6562–6566CrossRef Ambroise C, McLachlan GJ (2002) Selection bias in gene extraction on the basis of microarray gene-expression data. Proc Natl Acad Sci U S A 99:6562–6566CrossRef
41.
go back to reference Provost F, Domingos P (2003) Tree induction for probability-based ranking. Mach Learn 52:199–215CrossRef Provost F, Domingos P (2003) Tree induction for probability-based ranking. Mach Learn 52:199–215CrossRef
42.
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
43.
go back to reference Ortiz-Ramon R, Larroza A, Arana E, Moratal D (2017) Identifying the primary site of origin of MRI brain metastases from lung and breast cancer following a 2D radiomics approach. In: 2017 I.E. 14th International Symposium on Biomedical Imaging (ISBI 2017). Melbourne, VIC, pp 1213–1216 Ortiz-Ramon R, Larroza A, Arana E, Moratal D (2017) Identifying the primary site of origin of MRI brain metastases from lung and breast cancer following a 2D radiomics approach. In: 2017 I.E. 14th International Symposium on Biomedical Imaging (ISBI 2017). Melbourne, VIC, pp 1213–1216
44.
go back to reference Ortiz-Ramon R, Larroza A, Arana E, Moratal D (2017) A radiomics evaluation of 2D and 3D MRI texture features to classify brain metastases from lung cancer and melanoma. In: 2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Seogwipo, pp 493–496 Ortiz-Ramon R, Larroza A, Arana E, Moratal D (2017) A radiomics evaluation of 2D and 3D MRI texture features to classify brain metastases from lung cancer and melanoma. In: 2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Seogwipo, pp 493–496
45.
go back to reference Béresová M, Larroza A, Arana E, et al (2017) 2D and 3D texture analysis to differentiate brain metastases on MR images: proceed with caution. MAGMA 1–10 Béresová M, Larroza A, Arana E, et al (2017) 2D and 3D texture analysis to differentiate brain metastases on MR images: proceed with caution. MAGMA 1–10
46.
go back to reference Ahmed A, Gibbs P, Pickles M, Turnbull L (2013) Texture analysis in assessment and prediction of chemotherapy response in breast cancer. J Magn Reson Imaging 38:89–101CrossRef Ahmed A, Gibbs P, Pickles M, Turnbull L (2013) Texture analysis in assessment and prediction of chemotherapy response in breast cancer. J Magn Reson Imaging 38:89–101CrossRef
47.
go back to reference Chen W, Giger ML, Li H et al (2007) Volumetric texture analysis of breast lesions on contrast-enhanced magnetic resonance images. Magn Reson Med 58:562–571CrossRef Chen W, Giger ML, Li H et al (2007) Volumetric texture analysis of breast lesions on contrast-enhanced magnetic resonance images. Magn Reson Med 58:562–571CrossRef
Metadata
Title
Classifying brain metastases by their primary site of origin using a radiomics approach based on texture analysis: a feasibility study
Authors
Rafael Ortiz-Ramón
Andrés Larroza
Silvia Ruiz-España
Estanislao Arana
David Moratal
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 11/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5463-6

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