Deep Learning Approaches with Digital Mammography for Evaluating Breast Cancer Risk, a Narrative Review
Abstract
:1. Introduction
1.1. Screening Guidelines
1.2. Cancer Risk Models
1.3. Imaging Features for Risk Evaluation
1.4. AI and Risk Assessment
2. Methods
3. Study Selection
3.1. Small Scale Studies
3.2. Towards Clinical Validation
3.3. Novel Applications of DL Models beyond Screening
4. Discussion
4.1. Screening Implications
4.2. Summary and Future Direction
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer Statistics, 2017. CA Cancer J. Clin. 2017, 67, 7–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Madigan, M.P.; Ziegler, R.G.; Benichou, J.; Byrne, C.; Hoover, R.N. Proportion of breast cancer cases in the United States explained by well-established risk factors. J. Natl. Cancer Inst. 1995, 87, 1681–1685. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Narod, S.A.; Foulkes, W.D. BRCA1 and BRCA2: 1994 and beyond. Nat. Rev. Cancer 2004, 4, 665–676. [Google Scholar] [CrossRef] [PubMed]
- Acciavatti, R.J.; Lee, S.H.; Reig, B.; Moy, L.; Conant, E.F.; Kontos, D.; Moon, W.K. Beyond Breast Density: Risk Measures for Breast Cancer in Multiple Imaging Modalities. Radiology 2023, 306, e222575. [Google Scholar] [CrossRef] [PubMed]
- Gastounioti, A.; Desai, S.; Ahluwalia, V.S.; Conant, E.F.; Kontos, D. Artificial intelligence in mammographic phenotyping of breast cancer risk: A narrative review. Breast Cancer Res. 2022, 24, 14. [Google Scholar] [CrossRef]
- Siu, A.L.U.S. Preventive Services Task Force. Screening for Breast Cancer: U.S. Preventive Services Task Force Recommendation Statement. Ann. Intern. Med. 2016, 164, 279–296. [Google Scholar] [CrossRef] [Green Version]
- Bakker, M.F.; de Lange, S.V.; Pijnappel, R.M.; Mann, R.M.; Peeters, P.H.; Monninkhof, E.M.; Emaus, M.J.; Loo, C.E.; Bisschops, R.H.; Lobbes, M.B.; et al. Supplemental MRI Screening for Women with Extremely Dense Breast Tissue. N. Engl. J. Med. 2019, 381, 2091–2102. [Google Scholar] [CrossRef]
- Gail, M.H.; Brinton, L.A.; Byar, D.P.; Corle, D.K.; Green, S.B.; Schairer, C.; Mulvihill, J.J. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J. Natl. Cancer Inst. 1989, 81, 1879–1886. [Google Scholar] [CrossRef]
- Shieh, Y.; Hu, D.; Ma, L.; Huntsman, S.; Gard, C.C.; Leung, J.W.T.; Tice, J.A.; Vachon, C.M.; Cummings, S.R.; Kerlikowske, K.; et al. Breast cancer risk prediction using a clinical risk model and polygenic risk score. Breast Cancer Res. Treat. 2016, 159, 513–525. [Google Scholar] [CrossRef] [Green Version]
- Schonberg, M.A.; Karamourtopoulos, M.; Pinheiro, A.; Davis, R.B.; Sternberg, S.B.; Mehta, T.S.; Gilliam, E.A.; Tung, N.M. Variation in Breast Cancer Risk Model Estimates Among Women in Their 40s Seen in Primary Care. J. Womens Health 2022, 31, 495–502. [Google Scholar] [CrossRef]
- Kim, G.; Bahl, M. Assessing Risk of Breast Cancer: A Review of Risk Prediction Models. J. Breast Imaging 2021, 3, 144–155. [Google Scholar] [CrossRef]
- Vachon, C.M.; Brandt, K.R.; Ghosh, K.; Scott, C.G.; Maloney, S.D.; Carston, M.J.; Pankratz, V.S.; Sellers, T.A. Mammographic breast density as a general marker of breast cancer risk. Cancer Epidemiol. Biomark. Prev. 2007, 16, 43–49. [Google Scholar] [CrossRef] [Green Version]
- Kerlikowske, K.; Miglioretti, D.L.; Vachon, C.M. Discussions of Dense Breasts, Breast Cancer Risk, and Screening Choices in 2019. JAMA 2019, 322, 69–70. [Google Scholar] [CrossRef] [PubMed]
- Tice, J.A.; Cummings, S.R.; Smith-Bindman, R.; Ichikawa, L.; Barlow, W.E.; Kerlikowske, K. Using clinical factors and mammographic breast density to estimate breast cancer risk: Development and validation of a new predictive model. Ann. Intern. Med. 2008, 148, 337–347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Amir, E.; Freedman, O.C.; Seruga, B.; Evans, D.G. Assessing women at high risk of breast cancer: A review of risk assessment models. J. Natl. Cancer Inst. 2010, 102, 680–691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dembrower, K.; Liu, Y.; Azizpour, H.; Eklund, M.; Smith, K.; Lindholm, P.; Strand, F. Comparison of a Deep Learning Risk Score and Standard Mammographic Density Score for Breast Cancer Risk Prediction. Radiology 2020, 294, 265–272. [Google Scholar] [CrossRef] [PubMed]
- Ha, R.; Mutasa, S.; Sant EP, V.; Karcich, J.; Chin, C.; Liu, M.Z.; Jambawalikar, S. Accuracy of distinguishing atypical ductal hyperplasia from ductal carcinoma in situ with convolutional neural network–based machine learning approach using Mammographic Image Data. Am. J. Roentgenol. 2019, 212, 1166–1171. [Google Scholar] [CrossRef]
- Yala, A.; Lehman, C.; Schuster, T.; Portnoi, T.; Barzilay, R. A Deep Learning Mammography-based Model for Improved Breast Cancer Risk Prediction. Radiology 2019, 292, 60–66. [Google Scholar] [CrossRef] [Green Version]
- Manley, H.; Mutasa, S.; Chang, P.; Desperito, E.; Crew, K.; Ha, R. Dynamic Changes of Convolutional Neural Network-based Mammographic Breast Cancer Risk Score Among Women Undergoing Chemoprevention Treatment. Clin. Breast Cancer 2021, 21, e312–e318. [Google Scholar] [CrossRef]
- Arefan, D.; Mohamed, A.A.; Berg, W.A.; Zuley, M.L.; Sumkin, J.H.; Wu, S. Deep learning modeling using normal mammograms for predicting breast cancer risk. Med. Phys. 2020, 47, 110–118. [Google Scholar] [CrossRef] [Green Version]
- Kallenberg, M.; Petersen, K.; Nielsen, M.; Ng, A.Y.; Diao, P.; Igel, C.; Vachon, C.M.; Holland, K.; Winkel, R.R.; Karssemeijer, N.; et al. Unsupervised Deep Learning Applied to Breast Density Segmentation and Mammographic Risk Scoring. IEEE Trans. Med. Imaging 2016, 35, 1322–1331. [Google Scholar] [CrossRef] [PubMed]
- Maghsoudi, O.H.; Gastounioti, A.; Scott, C.; Pantalone, L.; Wu, F.-F.; Cohen, E.A.; Winham, S.; Conant, E.F.; Vachon, C.; Kontos, D. Deep-LIBRA: An artificial-intelligence method for robust quantification of breast density with independent validation in breast cancer risk assessment. Med. Image Anal. 2021, 73, 102138. [Google Scholar] [CrossRef] [PubMed]
- Michel, A.; Ro, V.; McGuinness, J.E.; Mutasa, S.; Terry, M.B.; Tehranifar, P.; May, B.; Ha, R.; Crew, K.D. Breast cancer risk prediction combining a convolutional neural network-based mammographic evaluation with clinical factors. Breast Cancer Res. Treat. 2023; online ahead of print. [Google Scholar] [CrossRef]
- Gastounioti, A.; Oustimov, A.; Hsieh, M.-K.; Pantalone, L.; Conant, E.F.; Kontos, D. Using Convolutional Neural Networks for Enhanced Capture of Breast Parenchymal Complexity Patterns Associated with Breast Cancer Risk. Acad. Radiol. 2018, 25, 977–984. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Giger, M.L.; Huynh, B.Q.; Antropova, N.O. Deep learning in breast cancer risk assessment: Evaluation of convolutional neural networks on a clinical dataset of full-field digital mammograms. J. Med. Imaging 2017, 4, 041304. [Google Scholar] [CrossRef]
- Wanders, J.O.P.; van Gils, C.H.; Karssemeijer, N.; Holland, K.; Kallenberg, M.; Peeters, P.H.M.; Nielsen, M.; Lillholm, M. The combined effect of mammographic texture and density on breast cancer risk: A cohort study. Breast Cancer Res. 2018, 20, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lehman, C.D.; Mercaldo, S.; Lamb, L.R.; King, A.T.; Ellisen, L.W.; Specht, M.; Tamimi, R.M. Deep Learning vs. Traditional Breast Cancer Risk Models to Support Risk-Based Mammography Screening. J. Natl. Cancer Inst. 2022, 114, 1355–1363. [Google Scholar] [CrossRef]
- Zhu, X.; Wolfgruber, T.K.; Leong, L.; Jensen, M.; Scott, C.; Winham, S.; Sadowski, P.; Vachon, C.; Kerlikowske, K.; Shepherd, J.A. Deep Learning Predicts Interval and Screening-detected Cancer from Screening Mammograms: A Case-Case-Control Study in 6369 Women. Radiology 2021, 301, 550–558. [Google Scholar] [CrossRef]
- Yala, A.; Mikhael, P.G.; Strand, F.; Lin, G.; Satuluru, S.; Kim, T.; Banerjee, I.; Gichoya, J.; Trivedi, H.; Lehman, C.D.; et al. Multi-Institutional Validation of a Mammography-Based Breast Cancer Risk Model. J. Clin. Oncol. 2022, 40, 1732–1740. [Google Scholar] [CrossRef]
- Ha, R.; Chang, P.; Karcich, J.; Mutasa, S.; Van Sant, E.P.; Liu, M.Z.; Jambawalikar, S. Convolutional Neural Network Based Breast Cancer Risk Stratification Using a Mammographic Dataset. Acad. Radiol. 2019, 26, 544–549. [Google Scholar] [CrossRef]
- McKinney, S.M.; Sieniek, M.; Godbole, V.; Godwin, J.; Antropova, N.; Ashrafian, H.; Back, T.; Chesus, M.; Corrado, G.S.; Darzi, A.; et al. International evaluation of an AI system for breast cancer screening. Nature 2020, 577, 89–94. [Google Scholar] [CrossRef]
- McGuinness, J.E.; Ro, V.; Mutasa, S.; Pan, S.; Hu, J.; Trivedi, M.S.; Accordino, M.K.; Kalinsky, K.; Hershman, D.L.; Ha, R.S.; et al. Use of a convolutional neural network-based mammographic evaluation to predict breast cancer recurrence among women with hormone receptor-positive operable breast cancer. Breast Cancer Res. Treat. 2022, 194, 35–47. [Google Scholar] [CrossRef] [PubMed]
Exams | Patients | Metric | Method | |
---|---|---|---|---|
Arefan, 2020 [20] | 226 | 226 (113) | 0.73 AUC |
8 Layer Inception CNN |
Gastounioti, 2018 [24] | 424 | 424 (106) | 0.90 AUC |
2 Layer CNN with CTA |
Li, 2017 [25] | 456 | 456 (75) | 0.84 AUC | 8 Layer CNN |
Ha, 2019 [30] | 1474 | 737 (210) | 0.72 Accuracy |
21 Layer Resnet CNN |
Kallenberg, 2016 [21] | 2069 | 2069 (394) | 0.57 AUC | 4 Layer CNN |
Zhu, 2021 [28] | 6369 | 6369 (278) | 0.72 C-index | 4 Layer CNN |
Dembrowser, 2020 [16] | 14,034 | 2283 (278) | 0.65 AUC | Inceptionv2 CNN+RF |
Michel, 2023 [23] | 23,467 (121) | 0.654 AUC |
21 Layer Resnet CNN | |
McKinney, 2020 [31] | 28,953 (1100) | 0.889 AUC | DL model | |
Yala, 2019 [18] | 88,994 | 39,571 | 0.70 AUC | 19 Layer Resnet CNN with transformers +RF |
Wanders, 2018 [26] | 51,400 (898) | 51,400 (898) | 0.61 C-index | 3 Layer CNN |
Lehman, 2022 [27] | 119,139 | 57,635 | 0.68 AUC | 19 Layer Resnet CNN with transformers +RF |
Yala, 2022 [29] | 19 Layer Resnet CNN with transformers +RF | |||
MGH | 25,855 (588) | 7005 (233) | 0.75 C-index | |
Novant | 14,157 (235) | 5887 (123) | 0.75 C-index | |
Emory | 44,008 (1003) | 16,495 (495) | 0.77 C-index | |
Maccabi Assuta | 6187 (186) | 6189 (186) | 0.77 C-index | |
Karolinska | 19,328 (1413) | 7353 (799) | 0.81 C-index | |
CGMH | 13,356 (244) | 13,356 (244) | 0.79 C-index | |
Barretos | 5900 (146) | 5900 (146) | 0.84 C-index |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Siddique, M.; Liu, M.; Duong, P.; Jambawalikar, S.; Ha, R. Deep Learning Approaches with Digital Mammography for Evaluating Breast Cancer Risk, a Narrative Review. Tomography 2023, 9, 1110-1119. https://doi.org/10.3390/tomography9030091
Siddique M, Liu M, Duong P, Jambawalikar S, Ha R. Deep Learning Approaches with Digital Mammography for Evaluating Breast Cancer Risk, a Narrative Review. Tomography. 2023; 9(3):1110-1119. https://doi.org/10.3390/tomography9030091
Chicago/Turabian StyleSiddique, Maham, Michael Liu, Phuong Duong, Sachin Jambawalikar, and Richard Ha. 2023. "Deep Learning Approaches with Digital Mammography for Evaluating Breast Cancer Risk, a Narrative Review" Tomography 9, no. 3: 1110-1119. https://doi.org/10.3390/tomography9030091
APA StyleSiddique, M., Liu, M., Duong, P., Jambawalikar, S., & Ha, R. (2023). Deep Learning Approaches with Digital Mammography for Evaluating Breast Cancer Risk, a Narrative Review. Tomography, 9(3), 1110-1119. https://doi.org/10.3390/tomography9030091