Multiregional Radiomic Signatures Based on Functional Parametric Maps from DCE-MRI for Preoperative Identification of Estrogen Receptor and Progesterone Receptor Status in Breast Cancer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients
2.2. Pathological Evaluation
2.3. MRI Acquisition
2.4. Tumor Segmentation
2.5. Calculation of Functional Parametric Maps
2.6. Feature Extraction
2.7. Interobserver Variability Assessment
2.8. Feature Selection and RS Establishment
2.9. Statistical Analysis
3. Results
3.1. Patient Characteristics
3.2. Feature Selection and RS Establishment
3.3. Radiomic Assessment
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Jensen, E.V.; Jordan, V.C. The estrogen receptor: A model for molecular medicine. Clin. Cancer Res. 2003, 9, 1980–1989. [Google Scholar]
- Horwitz, K.B.; McGuire, W.L. Predicting response to endocrine therapy in human breast cancer: A hypothesis. Science 1975, 189, 726–727. [Google Scholar] [CrossRef] [PubMed]
- Hilton, H.N.; Clarke, C.L.; Graham, J.D. Estrogen and progesterone signalling in the normal breast and its implications for cancer development. Mol. Cell. Endocrinol. 2018, 466, 2–14. [Google Scholar] [CrossRef] [PubMed]
- Győrffy, B.; Hatzis, C.; Sanft, T.; Hofstatter, E.; Aktas, B.; Pusztai, L. Multigene prognostic tests in breast cancer: Past, present, future. Breast Cancer Res. 2015, 17, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prat, A.; Ellis, M.J.; Perou, C.M. Practical implications of gene-expression-based assays for breast oncologists. Nat. Rev. Clin. Oncol. 2011, 9, 48–57. [Google Scholar] [CrossRef] [Green Version]
- Zaha, D.C. Significance of immunohistochemistry in breast cancer. World J. Clin. Oncol. 2014, 5, 382–392. [Google Scholar] [CrossRef] [PubMed]
- Demircioglu, A.; Grueneisen, J.; Ingenwerth, M.; Hoffmann, O.; Pinker-Domenig, K.; Morris, E.; Haubold, J.; Forsting, M.; Nensa, F.; Umutlu, L. A rapid volume of interest-based approach of radiomics analysis of breast MRI for tumor decoding and phenotyping of breast cancer. PLoS ONE 2020, 15, e0234871. [Google Scholar] [CrossRef]
- Sitaula, C.; Aryal, S. Fusion of whole and part features for the classification of histopathological image of breast tissue. Health Inf. Sci. Syst. 2020, 8, 38. [Google Scholar] [CrossRef]
- Aerts, H.J.W.L. The Potential of Radiomic-Based Phenotyping in Precision Medicine: A Review. JAMA Oncol. 2016, 2, 1636–1642. [Google Scholar] [CrossRef]
- Kuo, M.D.; Jamshidi, N. Behind the numbers: Decoding molecular phenotypes with radiogenomics—Guiding principles and technical considerations. Radiology 2014, 270, 320–325. [Google Scholar] [CrossRef] [PubMed]
- La Forgia, D.; Fanizzi, A.; Campobasso, F.; Bellotti, R.; Didonna, V.; Lorusso, V.; Moschetta, M.; Massafra, R.; Tamborra, P.; Tangaro, S.; et al. Radiomic Analysis in Contrast-Enhanced Spectral Mammography for Predicting Breast Cancer Histological Outcome. Diagnostics 2020, 10, 708. [Google Scholar] [CrossRef] [PubMed]
- Monti, S.; Aiello, M.; Incoronato, M.; Grimaldi, A.M.; Moscarino, M.; Mirabelli, P.; Ferbo, U.; Cavaliere, C.; Salvatore, M. DCE-MRI Pharmacokinetic-Based Phenotyping of Invasive Ductal Carcinoma: A Radiomic Study for Prediction of Histological Outcomes. Contrast Media Mol. Imaging 2018, 2018, 5076269. [Google Scholar] [CrossRef] [PubMed]
- Mao, Y.; Keller, E.T.; Garfield, D.H.; Shen, K.; Wang, J. Stromal cells in tumor microenvironment and breast cancer. Cancer Metastasis Rev. 2013, 32, 303–315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hattangadi, J.; Park, C.; Rembert, J.; Klifa, C.; Hwang, J.; Gibbs, J.; Hylton, N. Breast stromal enhancement on MRI is associated with response to neoadjuvant chemotherapy. Am. J. Roentgenol. 2008, 190, 1630–1636. [Google Scholar] [CrossRef]
- Kim, S.-A.; Cho, N.; Ryu, E.B.; Seo, M.; Bae, M.S.; Chang, J.M.; Moon, W.K. Background parenchymal signal enhancement ratio at preoperative MR imaging: Association with subsequent local recurrence in patients with ductal carcinoma in situ after breast conservation surgery. Radiology 2014, 270, 699–707. [Google Scholar] [CrossRef]
- Wu, J.; Li, B.; Sun, X.; Cao, G.; Rubin, D.L.; Napel, S.; Ikeda, D.M.; Kurian, A.W.; Li, R. Heterogeneous Enhancement Patterns of Tumor-adjacent Parenchyma at MR Imaging Are Associated with Dysregulated Signaling Pathways and Poor Survival in Breast Cancer. Radiology 2017, 285, 401–413. [Google Scholar] [CrossRef] [Green Version]
- Li, C.; Song, L.; Yin, J. Intratumoral and Peritumoral Radiomics Based on Functional Parametric Maps from Breast DCE-MRI for Prediction of HER-2 and Ki-67 Status. J. Magn. Reson. Imaging 2021, 54, 703–714. [Google Scholar] [CrossRef]
- Liu, C.; Ding, J.; Spuhler, K.; Gao, Y.; Serrano Sosa, M.; Moriarty, M.; Hussain, S.; He, X.; Liang, C.; Huang, C. Preoperative prediction of sentinel lymph node metastasis in breast cancer by radiomic signatures from dynamic contrast-enhanced MRI. J. Magn. Reson. Imaging 2019, 49, 131–140. [Google Scholar] [CrossRef] [Green Version]
- Boonyaratanakornkit, V.; McGowan, E.M.; Márquez-Garbán, D.C.; Burton, L.P.; Hamilton, N.; Pateetin, P.; Pietras, R.J. Progesterone Receptor Signaling in the Breast Tumor Microenvironment. Adv. Exp. Med. Biol. 2021, 1329, 443–474. [Google Scholar]
- Nie, P.; Yang, G.; Wang, Z.; Yan, L.; Miao, W.; Hao, D.; Wu, J.; Zhao, Y.; Gong, A.; Cui, J.; et al. A CT-based radiomics nomogram for differentiation of renal angiomyolipoma without visible fat from homogeneous clear cell renal cell carcinoma. Eur. Radiol. 2020, 30, 1274–1284. [Google Scholar] [CrossRef] [PubMed]
- Hammond, M.E.H.; Hayes, D.F.; Dowsett, M.; Allred, D.C.; Hagerty, K.L.; Badve, S.; Fitzgibbons, P.L.; Francis, G.; Goldstein, N.S.; Hayes, M.; et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J. Clin. Oncol. 2010, 28, 2784–2795. [Google Scholar] [CrossRef] [PubMed]
- Wolff, A.C.; Hammond, M.E.H.; Hicks, D.G.; Dowsett, M.; McShane, L.M.; Allison, K.H.; Allred, D.C.; Bartlett, J.M.S.; Bilous, M.; Fitzgibbons, P.; et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J. Clin. Oncol. 2013, 31, 3997–4013. [Google Scholar] [CrossRef] [PubMed]
- Tunali, I.; Stringfield, O.; Guvenis, A.; Wang, H.; Liu, Y.; Balagurunathan, Y.; Lambin, P.; Gillies, R.J.; Schabath, M.B. Radial gradient and radial deviation radiomic features from pre-surgical CT scans are associated with survival among lung adenocarcinoma patients. Oncotarget 2017, 8, 96013–96026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collewet, G.; Strzelecki, M.; Mariette, F. Influence of MRI acquisition protocols and image intensity normalization methods on texture classification. Magn. Reson. Imaging 2004, 22, 81–91. [Google Scholar] [CrossRef]
- Wang, H.; Nie, P.; Wang, Y.; Xu, W.; Duan, S.; Chen, H.; Hao, D.; Liu, J. Radiomics nomogram for differentiating between benign and malignant soft-tissue masses of the extremities. J. Magn. Reson. Imaging 2020, 51, 155–163. [Google Scholar] [CrossRef]
- Gibbs, P.; Turnbull, L.W. Textural analysis of contrast-enhanced MR images of the breast. Magn. Reson. Med. 2003, 50, 92–98. [Google Scholar] [CrossRef]
- Tang, T.-Y.; Li, X.; Zhang, Q.; Guo, C.-X.; Zhang, X.-Z.; Lao, M.-Y.; Shen, Y.-N.; Xiao, W.-B.; Ying, S.-H.; Sun, K.; et al. Development of a Novel Multiparametric MRI Radiomic Nomogram for Preoperative Evaluation of Early Recurrence in Resectable Pancreatic Cancer. J. Magn. Reson. Imaging 2020, 52, 231–245. [Google Scholar] [CrossRef] [Green Version]
- Liu, Z.; Zhang, X.-Y.; Shi, Y.-J.; Wang, L.; Zhu, H.-T.; Tang, Z.; Wang, S.; Li, X.-T.; Tian, J.; Sun, Y.-S. Radiomics Analysis for Evaluation of Pathological Complete Response to Neoadjuvant Chemoradiotherapy in Locally Advanced Rectal Cancer. Clin. Cancer Res. 2017, 23, 7253–7262. [Google Scholar] [CrossRef] [Green Version]
- Yu, X.; Song, W.; Guo, D.; Liu, H.; Zhang, H.; He, X.; Song, J.; Zhou, J.; Liu, X. Preoperative Prediction of Extramural Venous Invasion in Rectal Cancer: Comparison of the Diagnostic Efficacy of Radiomics Models and Quantitative Dynamic Contrast-Enhanced Magnetic Resonance Imaging. Front. Oncol. 2020, 10, 459. [Google Scholar] [CrossRef]
- Gillies, R.J.; Kinahan, P.E.; Hricak, H. Radiomics: Images Are More than Pictures, They Are Data. Radiology 2016, 278, 563–577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pilewskie, M.; Morrow, M. Applications for breast magnetic resonance imaging. Surg. Oncol. Clin. N. Am. 2014, 23, 431–449. [Google Scholar] [CrossRef] [PubMed]
- Mainiero, M.B.; Lourenco, A.; Mahoney, M.C.; Newell, M.S.; Bailey, L.; Barke, L.D.; D’Orsi, C.; Harvey, J.A.; Hayes, M.K.; Huynh, P.T.; et al. ACR Appropriateness Criteria Breast Cancer Screening. J. Am. Coll. Radiol. 2016, 13, R45–R49. [Google Scholar] [CrossRef]
- Li, C.; Yin, J. Radiomics Nomogram Based on Radiomics Score from Multiregional Diffusion-Weighted MRI and Clinical Factors for Evaluating HER-2 2+ Status of Breast Cancer. Diagnostics 2021, 11, 1491. [Google Scholar] [CrossRef] [PubMed]
- Braman, N.M.; Etesami, M.; Prasanna, P.; Dubchuk, C.; Gilmore, H.; Tiwari, P.; Plecha, D.; Madabhushi, A. Intratumoral and peritumoral radiomics for the pretreatment prediction of pathological complete response to neoadjuvant chemotherapy based on breast DCE-MRI. Breast Cancer Res. 2017, 19, 57. [Google Scholar] [CrossRef] [Green Version]
- Braman, N.; Prasanna, P.; Whitney, J.; Singh, S.; Beig, N.; Etesami, M.; Bates, D.D.B.; Gallagher, K.; Bloch, B.N.; Vulchi, M.; et al. Association of Peritumoral Radiomics with Tumor Biology and Pathologic Response to Preoperative Targeted Therapy for HER2 (ERBB2)-Positive Breast Cancer. JAMA Netw. Open 2019, 2, e192561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, Q.; Lin, X.; Zhao, Y.; Li, L.; Yan, K.; Liang, D.; Sun, D.; Li, Z.-C. Deep Learning vs. Radiomics for Predicting Axillary Lymph Node Metastasis of Breast Cancer Using Ultrasound Images: Don’t Forget the Peritumoral Region. Front. Oncol. 2020, 10, 53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barker, J.; Hoogi, A.; Depeursinge, A.; Rubin, D.L. Automated classification of brain tumor type in whole-slide digital pathology images using local representative tiles. Med. Image Anal. 2016, 30, 60–71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vink, J.P.; Van Leeuwen, M.B.; Van Deurzen, C.H.M.; De Haan, G. Efficient nucleus detector in histopathology images. J. Microsc. 2013, 249, 124–135. [Google Scholar] [CrossRef] [Green Version]
- Shao, L.; Liu, Z.; Feng, L.; Lou, X.; Li, Z.; Zhang, X.-Y.; Wan, X.; Zhou, X.; Sun, K.; Zhang, D.-F.; et al. Multiparametric MRI and Whole Slide Image-Based Pretreatment Prediction of Pathological Response to Neoadjuvant Chemoradiotherapy in Rectal Cancer: A Multicenter Radiopathomic Study. Ann. Surg. Oncol. 2020, 27, 4296–4306. [Google Scholar] [CrossRef]
- Fan, M.; Yuan, W.; Zhao, W.; Xu, M.; Wang, S.; Gao, X.; Li, L. Joint Prediction of Breast Cancer Histological Grade and Ki-67 Expression Level Based on DCE-MRI and DWI Radiomics. IEEE J. Biomed. Health Inform. 2020, 24, 1632–1642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leithner, D.; Mayerhoefer, M.E.; Martinez, D.F.; Jochelson, M.S.; Morris, E.A.; Thakur, S.B.; Pinker, K. Non-Invasive Assessment of Breast Cancer Molecular Subtypes with Multiparametric Magnetic Resonance Imaging Radiomics. J. Clin. Med. 2020, 9, 1853. [Google Scholar] [CrossRef] [PubMed]
Characteristics | Number of Patients (%) |
---|---|
Tumor size | |
≤20 | 162 (36.57%) |
>20 | 281 (63.43%) |
ER status | |
Positive | 292 (65.91%) |
Negative | 151 (34.09%) |
PR status | |
Positive | 279 (62.98%) |
Negative | 164 (37.02%) |
Ki-67 level | |
High | 282 (63.66%) |
Low | 161 (36.34) |
Histological type | |
Invasive ductal carcinoma | 394 (88.94%) |
Invasive lobular carcinoma | 15 (3.39%) |
Ductal carcinoma in situ | 17 (3.84%) |
Phyllode carcinoma | 11 (2.48%) |
Papillary carcinoma | 6 (1.35%) |
Intratumoral RS | Peritumoral RS | Multiregional RS | ||||
---|---|---|---|---|---|---|
Metrics | Training Set | Validation Set | Training Set | Validation Set | Training Set | Validation Set |
AUC (95% CI) | 0.828 (0.784–0.865) | 0.791 (0.691–0.871) | 0.755 (0.707–0.799) | 0.733 (0.628–0.822) | 0.851 (0.809–0.886) | 0.833 (0.738–0.905) |
Sensitivity | 0.664 | 0.850 | 0.603 | 0.667 | 0.845 | 0.850 |
Specificity | 0.839 | 0.704 | 0.815 | 0.741 | 0.694 | 0.778 |
Intratumoral RS | Peritumoral RS | Multiregional RS | ||||
---|---|---|---|---|---|---|
Metrics | Training Set | Validation Set | Training Set | Validation Set | Training Set | Validation Set |
AUC (95% CI) | 0.816 (0.772–0.855) | 0.749 (0.645–0.836) | 0.806 (0.761–0.846) | 0.708 (0.600–0.800) | 0.848 (0.806–0.883) | 0.763 (0.660–0.848) |
Sensitivity | 0.707 | 0.632 | 0.761 | 0.351 | 0.788 | 0.912 |
Specificity | 0.761 | 0.867 | 0.709 | 0.967 | 0.769 | 0.533 |
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Zhong, S.; Wang, F.; Wang, Z.; Zhou, M.; Li, C.; Yin, J. Multiregional Radiomic Signatures Based on Functional Parametric Maps from DCE-MRI for Preoperative Identification of Estrogen Receptor and Progesterone Receptor Status in Breast Cancer. Diagnostics 2022, 12, 2558. https://doi.org/10.3390/diagnostics12102558
Zhong S, Wang F, Wang Z, Zhou M, Li C, Yin J. Multiregional Radiomic Signatures Based on Functional Parametric Maps from DCE-MRI for Preoperative Identification of Estrogen Receptor and Progesterone Receptor Status in Breast Cancer. Diagnostics. 2022; 12(10):2558. https://doi.org/10.3390/diagnostics12102558
Chicago/Turabian StyleZhong, Shiling, Fan Wang, Zhiying Wang, Minghui Zhou, Chunli Li, and Jiandong Yin. 2022. "Multiregional Radiomic Signatures Based on Functional Parametric Maps from DCE-MRI for Preoperative Identification of Estrogen Receptor and Progesterone Receptor Status in Breast Cancer" Diagnostics 12, no. 10: 2558. https://doi.org/10.3390/diagnostics12102558
APA StyleZhong, S., Wang, F., Wang, Z., Zhou, M., Li, C., & Yin, J. (2022). Multiregional Radiomic Signatures Based on Functional Parametric Maps from DCE-MRI for Preoperative Identification of Estrogen Receptor and Progesterone Receptor Status in Breast Cancer. Diagnostics, 12(10), 2558. https://doi.org/10.3390/diagnostics12102558