Journal Article
. 2017 Jun; 7(1):4172.
doi: 10.1038/s41598-017-04075-z.

Breast Cancer Multi-classification from Histopathological Images with Structured Deep Learning Model

Zhongyi Han 1 Benzheng Wei 2 Yuanjie Zheng 3 Yilong Yin 4 Kejian Li 5 Shuo Li 6 
Affiliations
  • PMID: 28646155
  •     16 References
  •     41 citations

Abstract

Automated breast cancer multi-classification from histopathological images plays a key role in computer-aided breast cancer diagnosis or prognosis. Breast cancer multi-classification is to identify subordinate classes of breast cancer (Ductal carcinoma, Fibroadenoma, Lobular carcinoma, etc.). However, breast cancer multi-classification from histopathological images faces two main challenges from: (1) the great difficulties in breast cancer multi-classification methods contrasting with the classification of binary classes (benign and malignant), and (2) the subtle differences in multiple classes due to the broad variability of high-resolution image appearances, high coherency of cancerous cells, and extensive inhomogeneity of color distribution. Therefore, automated breast cancer multi-classification from histopathological images is of great clinical significance yet has never been explored. Existing works in literature only focus on the binary classification but do not support further breast cancer quantitative assessment. In this study, we propose a breast cancer multi-classification method using a newly proposed deep learning model. The structured deep learning model has achieved remarkable performance (average 93.2% accuracy) on a large-scale dataset, which demonstrates the strength of our method in providing an efficient tool for breast cancer multi-classification in clinical settings.

Deep MRI brain extraction: A 3D convolutional neural network for skull stripping.
Jens Kleesiek, Gregor Urban, +4 authors, Armin Biller.
Neuroimage, 2016 Jan 26; 129. PMID: 26808333
Highly Cited.
Deep convolutional neural networks for multi-modality isointense infant brain image segmentation.
Wenlu Zhang, Rongjian Li, +4 authors, Dinggang Shen.
Neuroimage, 2015 Jan 07; 108. PMID: 25562829    Free PMC article.
Highly Cited.
Multi-modal vertebrae recognition using Transformed Deep Convolution Network.
Yunliang Cai, Mark Landis, +3 authors, Shuo Li.
Comput Med Imaging Graph, 2016 Apr 23; 51. PMID: 27104497
Measuring sparse temporal-variation for accurate registration of dynamic contrast-enhanced breast MR images.
Yuanjie Zheng, Benzheng Wei, +2 authors, James C Gee.
Comput Med Imaging Graph, 2015 Jul 18; 46 Pt 1. PMID: 26183649
Neocognitron: a self organizing neural network model for a mechanism of pattern recognition unaffected by shift in position.
K Fukushima.
Biol Cybern, 1980 Jan 01; 36(4). PMID: 7370364
Highly Cited.
Hierarchical feature representation and multimodal fusion with deep learning for AD/MCI diagnosis.
Heung-Il Suk, Seong-Whan Lee, Dinggang Shen, Alzheimer's Disease Neuroimaging Initiative.
Neuroimage, 2014 Jul 22; 101. PMID: 25042445    Free PMC article.
Highly Cited.
A new initiative on precision medicine.
Francis S Collins, Harold Varmus.
N Engl J Med, 2015 Jan 31; 372(9). PMID: 25635347    Free PMC article.
Highly Cited.
Fast automated cell phenotype image classification.
Nicholas A Hamilton, Radosav S Pantelic, Kelly Hanson, Rohan D Teasdale.
BMC Bioinformatics, 2007 Mar 31; 8. PMID: 17394669    Free PMC article.
De-enhancing the dynamic contrast-enhanced breast MRI for robust registration.
Yuanjie Zheng, Jingyi Yu, +3 authors, Dinggang Shen.
Med Image Comput Comput Assist Interv, 2007 Dec 07; 10(Pt 1). PMID: 18051148    Free PMC article.
Precision-medicine plan raises hopes.
Sara Reardon.
Nature, 2015 Jan 30; 517(7536). PMID: 25631425
Reducing the dimensionality of data with neural networks.
G E Hinton, R R Salakhutdinov.
Science, 2006 Jul 29; 313(5786). PMID: 16873662
Highly Cited.
A Dataset for Breast Cancer Histopathological Image Classification.
Fabio A Spanhol, Luiz S Oliveira, Caroline Petitjean, Laurent Heutte.
IEEE Trans Biomed Eng, 2015 Nov 06; 63(7). PMID: 26540668
Deep learning as a tool for increased accuracy and efficiency of histopathological diagnosis.
Geert Litjens, Clara I Sánchez, +7 authors, Jeroen van der Laak.
Sci Rep, 2016 May 24; 6. PMID: 27212078    Free PMC article.
Highly Cited.
Scalable High-Performance Image Registration Framework by Unsupervised Deep Feature Representations Learning.
Guorong Wu, Minjeong Kim, +2 authors, Dinggang Shen.
IEEE Trans Biomed Eng, 2015 Nov 10; 63(7). PMID: 26552069    Free PMC article.
Deep learning.
Yann LeCun, Yoshua Bengio, Geoffrey Hinton.
Nature, 2015 May 29; 521(7553). PMID: 26017442
Highly Cited. Review.
Receptive fields of single neurones in the cat's striate cortex.
D H HUBEL, T N WIESEL.
J Physiol, 1959 Oct 01; 148. PMID: 14403679    Free PMC article.
Highly Cited.
A deep neural network to assess spontaneous pain from mouse facial expressions.
Alexander H Tuttle, Mark J Molinaro, +5 authors, Mark J Zylka.
Mol Pain, 2018 Mar 17; 14. PMID: 29546805    Free PMC article.
Association of Pathological Fibrosis With Renal Survival Using Deep Neural Networks.
Vijaya B Kolachalama, Priyamvada Singh, +6 authors, Vipul C Chitalia.
Kidney Int Rep, 2018 May 05; 3(2). PMID: 29725651    Free PMC article.
Multiclass classification for skin cancer profiling based on the integration of heterogeneous gene expression series.
Juan Manuel Gálvez, Daniel Castillo, +4 authors, Ignacio Rojas.
PLoS One, 2018 May 12; 13(5). PMID: 29750795    Free PMC article.
Gastric Pathology Image Classification Using Stepwise Fine-Tuning for Deep Neural Networks.
Jia Qu, Nobuyuki Hiruta, +3 authors, Hidenori Sakanashi.
J Healthc Eng, 2018 Jul 24; 2018. PMID: 30034677    Free PMC article.
Oxidative DNA damage induced by ROS-modulating agents with the ability to target DNA: A comparison of the biological characteristics of citrus pectin and apple pectin.
Fahimeh Salehi, Hossein Behboudi, Gholamreza Kavoosi, Sussan K Ardestani.
Sci Rep, 2018 Sep 19; 8(1). PMID: 30224635    Free PMC article.
Machine Learning Methods for Histopathological Image Analysis.
Daisuke Komura, Shumpei Ishikawa.
Comput Struct Biotechnol J, 2018 Oct 03; 16. PMID: 30275936    Free PMC article.
Highly Cited. Review.
Deep Semi Supervised Generative Learning for Automated Tumor Proportion Scoring on NSCLC Tissue Needle Biopsies.
Ansh Kapil, Armin Meier, +4 authors, Nicolas Brieu.
Sci Rep, 2018 Nov 28; 8(1). PMID: 30478349    Free PMC article.
Integrating clinical, molecular, proteomic and histopathological data within the tissue context: tissunomics.
Santiago Ramón Y Cajal, Stefan Hümmer, +5 authors, Javier Hernandez-Losa.
Histopathology, 2019 Jan 23; 75(1). PMID: 30667539    Free PMC article.
Review.
ARA: accurate, reliable and active histopathological image classification framework with Bayesian deep learning.
Łukasz Rączkowski, Marcin Możejko, Joanna Zambonelli, Ewa Szczurek.
Sci Rep, 2019 Oct 06; 9(1). PMID: 31586139    Free PMC article.
Breast cancer histopathology image classification through assembling multiple compact CNNs.
Chuang Zhu, Fangzhou Song, +3 authors, Jun Liu.
BMC Med Inform Decis Mak, 2019 Oct 24; 19(1). PMID: 31640686    Free PMC article.
Using deep convolutional neural networks for multi-classification of thyroid tumor by histopathology: a large-scale pilot study.
Yunjun Wang, Qing Guan, +8 authors, Jun Xiang.
Ann Transl Med, 2019 Nov 09; 7(18). PMID: 31700904    Free PMC article.
Quantitative scoring of epithelial and mesenchymal qualities of cancer cells using machine learning and quantitative phase imaging.
Van Lam, Thanh Nguyen, +4 authors, Christopher Raub.
J Biomed Opt, 2020 Feb 20; 25(2). PMID: 32072775    Free PMC article.
Pan-Renal Cell Carcinoma classification and survival prediction from histopathology images using deep learning.
Sairam Tabibu, P K Vinod, C V Jawahar.
Sci Rep, 2019 Jul 22; 9(1). PMID: 31324828    Free PMC article.
Cancer diagnosis through a tandem of classifiers for digitized histopathological slides.
Daniel Lichtblau, Catalin Stoean.
PLoS One, 2019 Jan 17; 14(1). PMID: 30650087    Free PMC article.
Breast cancer histopathological image classification using convolutional neural networks with small SE-ResNet module.
Yun Jiang, Li Chen, Hai Zhang, Xiao Xiao.
PLoS One, 2019 Mar 30; 14(3). PMID: 30925170    Free PMC article.
Evaluation of Transfer Learning with Deep Convolutional Neural Networks for Screening Osteoporosis in Dental Panoramic Radiographs.
Ki-Sun Lee, Seok-Ki Jung, +2 authors, Jinwook Choi.
J Clin Med, 2020 Feb 07; 9(2). PMID: 32024114    Free PMC article.
Digital Image Analysis of Heterogeneous Tuberculosis Pulmonary Pathology in Non-Clinical Animal Models using Deep Convolutional Neural Networks.
Bryce C Asay, Blake Blue Edwards, +10 authors, Anne J Lenaerts.
Sci Rep, 2020 Apr 10; 10(1). PMID: 32269234    Free PMC article.
Breast Cancer Classification from Histopathological Images with Inception Recurrent Residual Convolutional Neural Network.
Md Zahangir Alom, Chris Yakopcic, +2 authors, Vijayan K Asari.
J Digit Imaging, 2019 Feb 14; 32(4). PMID: 30756265    Free PMC article.
Conventional Machine Learning and Deep Learning Approach for Multi-Classification of Breast Cancer Histopathology Images-a Comparative Insight.
Shallu Sharma, Rajesh Mehra.
J Digit Imaging, 2020 Jan 05; 33(3). PMID: 31900812    Free PMC article.
Artificial intelligence in digital breast pathology: Techniques and applications.
Asmaa Ibrahim, Paul Gamble, +4 authors, Emad A Rakha.
Breast, 2020 Jan 15; 49. PMID: 31935669    Free PMC article.
Review.
Machine learning in nephrology: scratching the surface.
Qi Li, Qiu-Ling Fan, +5 authors, Han-Yu Zhu.
Chin Med J (Engl), 2020 Feb 13; (6). PMID: 32049747    Free PMC article.
Review.
A hybrid unsupervised-Deep learning tandem for electrooculography time series analysis.
Ruxandra Stoean, Catalin Stoean, +5 authors, Gonzalo Joya.
PLoS One, 2020 Jul 22; 15(7). PMID: 32692779    Free PMC article.
Classification of Microarray Gene Expression Data Using an Infiltration Tactics Optimization (ITO) Algorithm.
Javed Zahoor, Kashif Zafar.
Genes (Basel), 2020 Jul 28; 11(7). PMID: 32708429    Free PMC article.
Histopathological Classification of Breast Cancer Images Using a Multi-Scale Input and Multi-Feature Network.
Taimoor Shakeel Sheikh, Yonghee Lee, Migyung Cho.
Cancers (Basel), 2020 Jul 30; 12(8). PMID: 32722111    Free PMC article.
Breast Cancer Histopathology Image Classification Using an Ensemble of Deep Learning Models.
Zabit Hameed, Sofia Zahia, +2 authors, Ana María Vanegas.
Sensors (Basel), 2020 Aug 09; 20(16). PMID: 32764398    Free PMC article.
Embedding of Genes Using Cancer Gene Expression Data: Biological Relevance and Potential Application on Biomarker Discovery.
Chi Tung Choy, Chi Hang Wong, Stephen Lam Chan.
Front Genet, 2019 Jan 22; 9. PMID: 30662451    Free PMC article.
Deep Learning Based Analysis of Histopathological Images of Breast Cancer.
Juanying Xie, Ran Liu, Joseph Luttrell, Chaoyang Zhang.
Front Genet, 2019 Mar 07; 10. PMID: 30838023    Free PMC article.
The transition module: a method for preventing overfitting in convolutional neural networks.
S Akbar, M Peikari, +2 authors, A L Martel.
Comput Methods Biomech Biomed Eng Imaging Vis, 2019 Jun 14; 7(3). PMID: 31192055    Free PMC article.
Spectral-Spatial Features Integrated Convolution Neural Network for Breast Cancer Classification.
Hiren K Mewada, Amit V Patel, +2 authors, Keyur Mahant.
Sensors (Basel), 2020 Aug 28; 20(17). PMID: 32842640    Free PMC article.
Fluorescence imaging and Raman spectroscopy applied for the accurate diagnosis of breast cancer with deep learning algorithms.
Lin-Wei Shang, Dan-Ying Ma, +4 authors, Jian-Hua Yin.
Biomed Opt Express, 2020 Oct 06; 11(7). PMID: 33014559    Free PMC article.
Computer-Aided Histopathological Image Analysis Techniques for Automated Nuclear Atypia Scoring of Breast Cancer: a Review.
Asha Das, Madhu S Nair, S David Peter.
J Digit Imaging, 2020 Jan 29; 33(5). PMID: 31989390    Free PMC article.
Review.
Fine-Grained Breast Cancer Classification With Bilinear Convolutional Neural Networks (BCNNs).
Weihuang Liu, Mario Juhas, Yang Zhang.
Front Genet, 2020 Oct 27; 11. PMID: 33101377    Free PMC article.
Ginseng polysaccharide inhibits MDA-MB-231 cell proliferation by activating the inflammatory response.
Haoliang Zhou, Yuxiang Yan, +3 authors, Ruokuo Han.
Exp Ther Med, 2020 Nov 06; 20(6). PMID: 33149784    Free PMC article.
Breast Microcalcification Diagnosis Using Deep Convolutional Neural Network from Digital Mammograms.
Hongmin Cai, Qinjian Huang, +5 authors, Li Li.
Comput Math Methods Med, 2019 Apr 05; 2019. PMID: 30944574    Free PMC article.
Deep neural network models for computational histopathology: A survey.
Chetan L Srinidhi, Ozan Ciga, Anne L Martel.
Med Image Anal, 2020 Oct 14; 67. PMID: 33049577    Free PMC article.
A Semisupervised Learning Scheme with Self-Paced Learning for Classifying Breast Cancer Histopathological Images.
Sarpong Kwadwo Asare, Fei You, Obed Tettey Nartey.
Comput Intell Neurosci, 2020 Dec 31; 2020. PMID: 33376479    Free PMC article.
Discovery and Proof-of-Concept Study of Nuclease Activity as a Novel Biomarker for Breast Cancer Tumors.
Luiza I Hernandez, Marcos J Araúzo-Bravo, +9 authors, Frank J Hernandez.
Cancers (Basel), 2021 Jan 17; 13(2). PMID: 33451046    Free PMC article.
Aggregation of cohorts for histopathological diagnosis with deep morphological analysis.
Jeonghyuk Park, Yul Ri Chung, +5 authors, Kyu-Hwan Jung.
Sci Rep, 2021 Feb 05; 11(1). PMID: 33536550    Free PMC article.
Artificial Intelligence & Tissue Biomarkers: Advantages, Risks and Perspectives for Pathology.
Cesare Lancellotti, Pierandrea Cancian, +4 authors, Luca Di Tommaso.
Cells, 2021 May 01; 10(4). PMID: 33918173    Free PMC article.
Review.
A fast and effective detection framework for whole-slide histopathology image analysis.
Jun Ruan, Zhikui Zhu, +3 authors, Junqiu Yue.
PLoS One, 2021 May 13; 16(5). PMID: 33979398    Free PMC article.
Artificial intelligence and machine learning for medical imaging: A technology review.
Ana Barragán-Montero, Umair Javaid, +11 authors, John A Lee.
Phys Med, 2021 May 13; 83. PMID: 33979715    Free PMC article.
Review.