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Published in: Journal of Translational Medicine 1/2021

Open Access 01-12-2021 | Breast Cancer | Research

Radiomics-based machine learning analysis and characterization of breast lesions with multiparametric diffusion-weighted MR

Authors: Kun Sun, Zhicheng Jiao, Hong Zhu, Weimin Chai, Xu Yan, Caixia Fu, Jie-Zhi Cheng, Fuhua Yan, Dinggang Shen

Published in: Journal of Translational Medicine | Issue 1/2021

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Abstract

Background

This study aimed to evaluate the utility of radiomics-based machine learning analysis with multiparametric DWI and to compare the diagnostic performance of radiomics features and mean diffusion metrics in the characterization of breast lesions.

Methods

This retrospective study included 542 lesions from February 2018 to November 2018. One hundred radiomics features were computed from mono-exponential (ME), biexponential (BE), stretched exponential (SE), and diffusion-kurtosis imaging (DKI). Radiomics-based analysis was performed by comparing four classifiers, including random forest (RF), principal component analysis (PCA), L1 regularization (L1R), and support vector machine (SVM). These four classifiers were trained on a training set with 271 patients via ten-fold cross-validation and tested on an independent testing set with 271 patients. The diagnostic performance of the mean diffusion metrics of ME (mADCall b, mADC0–1000), BE (mD, mD*, mf), SE (mDDC, mα), and DKI (mK, mD) were also calculated for comparison. The area under the receiver operating characteristic curve (AUC) was used to compare the diagnostic performance.

Results

RF attained higher AUCs than L1R, PCA and SVM. The AUCs of radiomics features for the differential diagnosis of breast lesions ranged from 0.80 (BE_D*) to 0.85 (BE_D). The AUCs of the mean diffusion metrics ranged from 0.54 (BE_mf) to 0.79 (ME_mADC0–1000). There were significant differences in the AUCs between the mean values of all diffusion metrics and radiomics features of AUCs (all P < 0.001) for the differentiation of benign and malignant breast lesions. Of the radiomics features computed, the most important sequence was BE_D (AUC: 0.85), and the most important feature was FO-10 percentile (Feature Importance: 0.04).

Conclusions

The radiomics-based analysis of multiparametric DWI by RF enables better differentiation of benign and malignant breast lesions than the mean diffusion metrics.
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Literature
1.
go back to reference Kuhl CK, Jost P, Morakkabati N, Zivanovic O, Schild HH, Gieseke J. Contrast-enhanced MR imaging of the breast at 3.0 and 1.5 T in the same patients: initial experience. Radiology. 2006;239:666–776.CrossRef Kuhl CK, Jost P, Morakkabati N, Zivanovic O, Schild HH, Gieseke J. Contrast-enhanced MR imaging of the breast at 3.0 and 1.5 T in the same patients: initial experience. Radiology. 2006;239:666–776.CrossRef
2.
go back to reference Uematsu T, Kasami M, Watanabe J. Does the degree of background enhancement in breast MRI affect the detection and staging of breast cancer? Eur Radiol. 2011;21:2261–7.CrossRef Uematsu T, Kasami M, Watanabe J. Does the degree of background enhancement in breast MRI affect the detection and staging of breast cancer? Eur Radiol. 2011;21:2261–7.CrossRef
3.
go back to reference Giess CS, Yeh ED, Raza S, Birdwell RL. Background parenchymal enhancement at breast MR imaging: normal patterns, diagnostic challenges, and potential for false-positive and false-negative interpretation. Radiographics. 2014;34:234–47.CrossRef Giess CS, Yeh ED, Raza S, Birdwell RL. Background parenchymal enhancement at breast MR imaging: normal patterns, diagnostic challenges, and potential for false-positive and false-negative interpretation. Radiographics. 2014;34:234–47.CrossRef
4.
go back to reference Song SE, Park EK, Cho KR, Seo BK, Woo OH, Jung SP. Additional value of diffusion-weighted imaging to evaluate multifocal and multicentric breast cancer detected using pre-operative breast MRI. Eur Radiol. 2017;27:4819–27.CrossRef Song SE, Park EK, Cho KR, Seo BK, Woo OH, Jung SP. Additional value of diffusion-weighted imaging to evaluate multifocal and multicentric breast cancer detected using pre-operative breast MRI. Eur Radiol. 2017;27:4819–27.CrossRef
5.
go back to reference Spick C, Pinker-Domenig K, Rudas M, Helbich TH, Baltzer PA. MRI-only lesions: application of diffusion-weighted imaging obviates unnecessary MR-guided breast biopsies. Eur Radiol. 2014;24:1204–10.CrossRef Spick C, Pinker-Domenig K, Rudas M, Helbich TH, Baltzer PA. MRI-only lesions: application of diffusion-weighted imaging obviates unnecessary MR-guided breast biopsies. Eur Radiol. 2014;24:1204–10.CrossRef
6.
go back to reference Kul S, Cansu A, Alhan E, Dinc H, Gunes G, Reis A. Contribution of diffusion-weighted imaging to dynamic contrast-enhanced MRI in the characterization of breast tumors. Am J Roentgenol. 2011;196:210–7.CrossRef Kul S, Cansu A, Alhan E, Dinc H, Gunes G, Reis A. Contribution of diffusion-weighted imaging to dynamic contrast-enhanced MRI in the characterization of breast tumors. Am J Roentgenol. 2011;196:210–7.CrossRef
7.
go back to reference Liu C, Liang C, Liu Z, Zhang S, Huang B. Intravoxel incoherent motion (IVIM) in evaluation of breast lesions: comparison with conventional DWI. Eur J Radiol. 2013;82:e782–9.CrossRef Liu C, Liang C, Liu Z, Zhang S, Huang B. Intravoxel incoherent motion (IVIM) in evaluation of breast lesions: comparison with conventional DWI. Eur J Radiol. 2013;82:e782–9.CrossRef
8.
go back to reference Lai V, Lee VH, Lam KO, Sze HC, Chan Q, Khong PL. Intravoxel water diffusion heterogeneity MR imaging of nasopharyngeal carcinoma using stretched exponential diffusion model. Eur Radiol. 2015;25:1708–13.CrossRef Lai V, Lee VH, Lam KO, Sze HC, Chan Q, Khong PL. Intravoxel water diffusion heterogeneity MR imaging of nasopharyngeal carcinoma using stretched exponential diffusion model. Eur Radiol. 2015;25:1708–13.CrossRef
9.
go back to reference Sun K, Chen X, Chai W, Fei X, Fu C, Yan X. Breast cancer: diffusion kurtosis MR imaging-diagnostic accuracy and correlation with clinical-pathologic factors. Radiology. 2015;277:46–55.CrossRef Sun K, Chen X, Chai W, Fei X, Fu C, Yan X. Breast cancer: diffusion kurtosis MR imaging-diagnostic accuracy and correlation with clinical-pathologic factors. Radiology. 2015;277:46–55.CrossRef
10.
go back to reference Suo S, Yin Y, Geng X, Zhang D, Hua J, Cheng F, et al. Diffusion-weighted MRI for predicting pathologic response to neoadjuvant chemotherapy in breast cancer: evaluation with mono-, bi-, and stretched-exponential models. J Transl Med. 2021;19:1–12.CrossRef Suo S, Yin Y, Geng X, Zhang D, Hua J, Cheng F, et al. Diffusion-weighted MRI for predicting pathologic response to neoadjuvant chemotherapy in breast cancer: evaluation with mono-, bi-, and stretched-exponential models. J Transl Med. 2021;19:1–12.CrossRef
11.
go back to reference Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology. 1988;168:497–505.CrossRef Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology. 1988;168:497–505.CrossRef
12.
go back to reference Le Bihan D, Turner R, MacFall JR. Effects of intravoxel incoherent motions (IVIM) in steady-state free precession (SSFP) imaging: application to molecular diffusion imaging. Magn Reson Med. 1989;10:324–37.CrossRef Le Bihan D, Turner R, MacFall JR. Effects of intravoxel incoherent motions (IVIM) in steady-state free precession (SSFP) imaging: application to molecular diffusion imaging. Magn Reson Med. 1989;10:324–37.CrossRef
13.
go back to reference Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS. Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med. 2003;50:727–34.CrossRef Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS. Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med. 2003;50:727–34.CrossRef
14.
go back to reference Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432–40.CrossRef Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432–40.CrossRef
15.
go back to reference Suo S, Cheng F, Cao M, Kang J, Wang M, Hua J. Multiparametric diffusion-weighted imaging in breast lesions: association with pathologic diagnosis and prognostic factors. J Magn Reson Imaging. 2017;46:740–50.CrossRef Suo S, Cheng F, Cao M, Kang J, Wang M, Hua J. Multiparametric diffusion-weighted imaging in breast lesions: association with pathologic diagnosis and prognostic factors. J Magn Reson Imaging. 2017;46:740–50.CrossRef
16.
go back to reference Liu C, Wang K, Li X, Zhang J, Ding J, Spuhler K. Breast lesion characterization using whole-lesion histogram analysis with stretched-exponential diffusion model. J Magn Reson Imaging. 2018;47:1701–10.CrossRef Liu C, Wang K, Li X, Zhang J, Ding J, Spuhler K. Breast lesion characterization using whole-lesion histogram analysis with stretched-exponential diffusion model. J Magn Reson Imaging. 2018;47:1701–10.CrossRef
17.
go back to reference Bickelhaupt S, Jaeger PF, Laun FB, Lederer W, Daniel H, Kuder TA. Radiomics based on adapted diffusion kurtosis imaging helps to clarify most mammographic findings suspicious for cancer. Radiology. 2018;287:761–70.CrossRef Bickelhaupt S, Jaeger PF, Laun FB, Lederer W, Daniel H, Kuder TA. Radiomics based on adapted diffusion kurtosis imaging helps to clarify most mammographic findings suspicious for cancer. Radiology. 2018;287:761–70.CrossRef
18.
go back to reference Bahl M, Barzilay R, Yedidia AB, Locascio NJ, Yu L, Lehman CD. High-risk breast lesions: a machine learning model to predict pathologic upgrade and reduce unnecessary surgical excision. Radiology. 2018;286:810–8.CrossRef Bahl M, Barzilay R, Yedidia AB, Locascio NJ, Yu L, Lehman CD. High-risk breast lesions: a machine learning model to predict pathologic upgrade and reduce unnecessary surgical excision. Radiology. 2018;286:810–8.CrossRef
19.
go back to reference Kniep HC, Madesta F, Schneider T, Hanning U, Schonfeld MH, Schon G. Radiomics of brain MRI: utility in prediction of metastatic tumor type. Radiology. 2019;290:479–87.CrossRef Kniep HC, Madesta F, Schneider T, Hanning U, Schonfeld MH, Schon G. Radiomics of brain MRI: utility in prediction of metastatic tumor type. Radiology. 2019;290:479–87.CrossRef
20.
go back to reference Liu J, Sun D, Chen L, Fang Z, Song W, Guo D, et al. Radiomics analysis of dynamic contrast-enhanced magnetic resonance imaging for the prediction of sentinel lymph node metastasis in breast cancer. Front Oncol. 2019;9:980.CrossRef Liu J, Sun D, Chen L, Fang Z, Song W, Guo D, et al. Radiomics analysis of dynamic contrast-enhanced magnetic resonance imaging for the prediction of sentinel lymph node metastasis in breast cancer. Front Oncol. 2019;9:980.CrossRef
21.
go back to reference Liang C, Cheng Z, Huang Y, He L, Chen X, Ma Z. An MRI-based radiomics classifier for preoperative prediction of Ki-67 status in breast cancer. Acad Radiol. 2018;25:1111–7.CrossRef Liang C, Cheng Z, Huang Y, He L, Chen X, Ma Z. An MRI-based radiomics classifier for preoperative prediction of Ki-67 status in breast cancer. Acad Radiol. 2018;25:1111–7.CrossRef
22.
go back to reference Chai R, Ma H, Xu M, Arefan D, Cui X, Liu Y. Differentiating axillary lymph node metastasis in invasive breast cancer patients: a comparison of radiomic signatures from multiparametric breast MR sequences. J Magn Reson Imaging. 2019;50:1125–32.CrossRef Chai R, Ma H, Xu M, Arefan D, Cui X, Liu Y. Differentiating axillary lymph node metastasis in invasive breast cancer patients: a comparison of radiomic signatures from multiparametric breast MR sequences. J Magn Reson Imaging. 2019;50:1125–32.CrossRef
23.
go back to reference Truhn D, Schrading S, Haarburger C, Schneider H, Merhof D, Kuhl C. Radiomic versus convolutional neural networks analysis for classification of contrast-enhancing lesions at multiparametric breast MRI. Radiology. 2019;290:290–7.CrossRef Truhn D, Schrading S, Haarburger C, Schneider H, Merhof D, Kuhl C. Radiomic versus convolutional neural networks analysis for classification of contrast-enhancing lesions at multiparametric breast MRI. Radiology. 2019;290:290–7.CrossRef
24.
go back to reference Bonekamp D, Kohl S, Wiesenfarth M, Schelb P, Radtke JP, Gotz M. Radiomic machine learning for characterization of prostate lesions with MRI: comparison to ADC values. Radiology. 2018;289:128–37.CrossRef Bonekamp D, Kohl S, Wiesenfarth M, Schelb P, Radtke JP, Gotz M. Radiomic machine learning for characterization of prostate lesions with MRI: comparison to ADC values. Radiology. 2018;289:128–37.CrossRef
25.
go back to reference Dong Y, Feng Q, Yang W, Lu Z, Deng C, Zhang L. Preoperative prediction of sentinel lymph node metastasis in breast cancer based on radiomics of T2-weighted fat-suppression and diffusion-weighted MRI. Eur Radiol. 2018;28:582–91.CrossRef Dong Y, Feng Q, Yang W, Lu Z, Deng C, Zhang L. Preoperative prediction of sentinel lymph node metastasis in breast cancer based on radiomics of T2-weighted fat-suppression and diffusion-weighted MRI. Eur Radiol. 2018;28:582–91.CrossRef
26.
go back to reference van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.CrossRef van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.CrossRef
27.
go back to reference Gu D, Hu Y, Ding H, Wei J, Chen K, Liu H. CT radiomics may predict the grade of pancreatic neuroendocrine tumors: a multicenter study. Eur Radiol. 2019;29:6880–90.CrossRef Gu D, Hu Y, Ding H, Wei J, Chen K, Liu H. CT radiomics may predict the grade of pancreatic neuroendocrine tumors: a multicenter study. Eur Radiol. 2019;29:6880–90.CrossRef
28.
29.
go back to reference Chen S-Y, Feng Z, Yi X. A general introduction to adjustment for multiple comparisons. J Thorac Dis. 2017;9:1725.CrossRef Chen S-Y, Feng Z, Yi X. A general introduction to adjustment for multiple comparisons. J Thorac Dis. 2017;9:1725.CrossRef
30.
go back to reference Abraham A, Pedregosa F, Eickenberg M, Gervais P, Mueller A, Kossaifi J. Machine learning for neuroimaging with scikit-learn. Front Neuroinform. 2014;8:14.CrossRef Abraham A, Pedregosa F, Eickenberg M, Gervais P, Mueller A, Kossaifi J. Machine learning for neuroimaging with scikit-learn. Front Neuroinform. 2014;8:14.CrossRef
31.
go back to reference Woodard GA, Ray KM, Joe BN, Price ER. Qualitative radiogenomics: association between Oncotype DX test recurrence score and BI-RADS mammographic and breast MR imaging features. Radiology. 2018;286:60–70.CrossRef Woodard GA, Ray KM, Joe BN, Price ER. Qualitative radiogenomics: association between Oncotype DX test recurrence score and BI-RADS mammographic and breast MR imaging features. Radiology. 2018;286:60–70.CrossRef
32.
go back to reference Bickelhaupt S, Paech D, Kickingereder P, Steudle F, Lederer W, Daniel H. Prediction of malignancy by a radiomic signature from contrast agent-free diffusion MRI in suspicious breast lesions found on screening mammography. J Magn Reson Imaging. 2017;46:604–16.CrossRef Bickelhaupt S, Paech D, Kickingereder P, Steudle F, Lederer W, Daniel H. Prediction of malignancy by a radiomic signature from contrast agent-free diffusion MRI in suspicious breast lesions found on screening mammography. J Magn Reson Imaging. 2017;46:604–16.CrossRef
33.
go back to reference Bogner W, Pinker-Domenig K, Bickel H, Chmelik M, Weber M, Helbich TH. Readout-segmented echo-planar imaging improves the diagnostic performance of diffusion-weighted MR breast examinations at 3.0 T. Radiology. 2012;263:64–76.CrossRef Bogner W, Pinker-Domenig K, Bickel H, Chmelik M, Weber M, Helbich TH. Readout-segmented echo-planar imaging improves the diagnostic performance of diffusion-weighted MR breast examinations at 3.0 T. Radiology. 2012;263:64–76.CrossRef
34.
go back to reference Gruber S, Minarikova L, Pinker K, Zaric O, Chmelik M, Strasser B. Diffusion-weighted imaging of breast tumours at 3 Tesla and 7 Tesla: a comparison. Eur Radiol. 2016;26:1466–73.CrossRef Gruber S, Minarikova L, Pinker K, Zaric O, Chmelik M, Strasser B. Diffusion-weighted imaging of breast tumours at 3 Tesla and 7 Tesla: a comparison. Eur Radiol. 2016;26:1466–73.CrossRef
35.
go back to reference Ehteshami Bejnordi B, Veta M, Johannes van Diest P, van Ginneken B, Karssemeijer N, Litjens G. Diagnostic assessment of deep learning algorithms for detection of lymph node metastases in women with breast cancer. JAMA. 2017;318:2199–210.CrossRef Ehteshami Bejnordi B, Veta M, Johannes van Diest P, van Ginneken B, Karssemeijer N, Litjens G. Diagnostic assessment of deep learning algorithms for detection of lymph node metastases in women with breast cancer. JAMA. 2017;318:2199–210.CrossRef
36.
go back to reference Xie T, Wang Z, Zhao Q, Bai Q, Zhou X, Gu Y, et al. Machine learning-based analysis of MR multiparametric radiomics for the subtype classification of breast cancer. Front Oncol. 2019;9:505.CrossRef Xie T, Wang Z, Zhao Q, Bai Q, Zhou X, Gu Y, et al. Machine learning-based analysis of MR multiparametric radiomics for the subtype classification of breast cancer. Front Oncol. 2019;9:505.CrossRef
37.
go back to reference Fan M, Zhang P, Wang Y, Peng W, Wang S, Gao X. Radiomic analysis of imaging heterogeneity in tumours and the surrounding parenchyma based on unsupervised decomposition of DCE-MRI for predicting molecular subtypes of breast cancer. Eur Radiol. 2019;29:4456–67.CrossRef Fan M, Zhang P, Wang Y, Peng W, Wang S, Gao X. Radiomic analysis of imaging heterogeneity in tumours and the surrounding parenchyma based on unsupervised decomposition of DCE-MRI for predicting molecular subtypes of breast cancer. Eur Radiol. 2019;29:4456–67.CrossRef
38.
go back to reference Sutton EJ, Oh JH, Dashevsky BZ, Veeraraghavan H, Apte AP, Thakur SB. Breast cancer subtype intertumor heterogeneity: MRI-based features predict results of a genomic assay. J Magn Reson Imaging. 2015;42:1398–406.CrossRef Sutton EJ, Oh JH, Dashevsky BZ, Veeraraghavan H, Apte AP, Thakur SB. Breast cancer subtype intertumor heterogeneity: MRI-based features predict results of a genomic assay. J Magn Reson Imaging. 2015;42:1398–406.CrossRef
39.
go back to reference Kolarevic D, Tomasevic Z, Dzodic R, Kanjer K, Vukosavljevic DN, Radulovic M. Early prognosis of metastasis risk in inflammatory breast cancer by texture analysis of tumour microscopic images. Biomed Microdevices. 2015;17:92.CrossRef Kolarevic D, Tomasevic Z, Dzodic R, Kanjer K, Vukosavljevic DN, Radulovic M. Early prognosis of metastasis risk in inflammatory breast cancer by texture analysis of tumour microscopic images. Biomed Microdevices. 2015;17:92.CrossRef
40.
go back to reference Waugh SA, Purdie CA, Jordan LB, Vinnicombe S, Lerski RA, Martin P. Magnetic resonance imaging texture analysis classification of primary breast cancer. Eur Radiol. 2016;26:322–30.CrossRef Waugh SA, Purdie CA, Jordan LB, Vinnicombe S, Lerski RA, Martin P. Magnetic resonance imaging texture analysis classification of primary breast cancer. Eur Radiol. 2016;26:322–30.CrossRef
Metadata
Title
Radiomics-based machine learning analysis and characterization of breast lesions with multiparametric diffusion-weighted MR
Authors
Kun Sun
Zhicheng Jiao
Hong Zhu
Weimin Chai
Xu Yan
Caixia Fu
Jie-Zhi Cheng
Fuhua Yan
Dinggang Shen
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-03117-5

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