Abstract
Breast cancer (BrC) is the leading cause of abnormal death in women. Mammograms and histopathology (Hp) biopsy images are generally recommended for early diagnosis of BrC because Hp image-based diagnosis enables doctors to make cancer diagnostic decisions more confidently than with mammograms. Several studies have used Hp images to classify BrC. However, the performance of classification models is compromised due to the higher misclassification rate. Therefore, this study aimed to develop a reliable, accurate, and computationally cost-effective ensembled BrC classification network (EBrC-Net) model with three misclassification algorithms to diagnose breast malignancy in early stages using Hp images. The proposed EBrC-Net model is based on the deep convolutional neural network approach. For experiments, the publicly available BreakHis dataset was used and split into training, validation, and testing sets. In addition, image augmentation was adopted for the training set only, and features were extracted through the well-trained EBrC-Net. Thereafter, the extracted features were further evaluated by six machine learning classifiers, of which two best performing classifiers (i.e., softmax and k-nearest neighbour [kNN]) were selected on the basis of five performance metric evaluation results. Furthermore, three misclassification reduction (McR) algorithms were developed and implemented in cascaded manner to reduce the false predictions of the softmax and kNN classifiers. After the implementation of the McR algorithms, experiments showed that the kNN results were much better and reliable than the softmax. The proposed BrC classification model achieved accuracy, specificity, and sensitivity rates of 97.74%, 100%, and 97.01%, respectively. Moreover, the performance of proposed BrC classification model was compared with that of state-of-the-art baseline models. Findings showed that the proposed EBrC-Net classification model, coupled with the proposed McR algorithms, achieved the best results in comparison with the baseline classification models. The proposed EBrC-Net model and the McR algorithms are a reliable source for doctors aiming for second opinion in making early diagnostic decisions for BrC using Hp images.
Similar content being viewed by others
References
Abdullah-Al N, Bin Ali F, Kong YN (2017) Histopathological breast-image classification with image enhancement by convolutional neural network. Paper presented at the 2017 20th international conference of computer and information technology, New York
Aghdam MH, Heidari S (2015) Feature selection using particle swarm optimization in text categorization. Journal of Artificial Intelligence and Soft Computing Research 5(4):231–238
Allison KH, Reisch LM, Carney PA, Weaver DL, Schnitt SJ, O'Malley FP, … Elmore JG (2014) Understanding diagnostic variability in breast pathology: lessons learned from an expert consensus review panel. Histopathology 65(2):240–251. https://doi.org/10.1111/his.12387
Amit G, Ben-Ari R, Hadad O, Monovich E, Granot N, Hashoul S (2017) Classification of breast MRI lesions using small-size training sets: comparison of deep learning approaches. Paper presented at the Progress in Biomedical Optics and Imaging - Proceedings of SPIE
Araujo T, Aresta G, Castro E, Rouco J, Aguiar P, Eloy C, … Campilho A (2017) Classification of breast cancer histology images using convolutional neural networks. PLoS One 12(6):14. https://doi.org/10.1371/journal.pone.0177544
Arefan D, Talebpour A, Ahmadinejhad N, Asl AK (2015) Automatic breast density classification using neural network. J Instrum 10(12). https://doi.org/10.1088/1748-0221/10/12/T12002
Arevalo J, González FA, Ramos-Pollán R, Oliveira J L, Lopez MAG (2015) Convolutional neural networks for mammography mass lesion classification. Paper presented at the 2015 37th annual international conference of the IEEE engineering in medicine and biology society (EMBC)
Bardou D, Zhang K, Ahmad SM (2018) Classification of breast cancer based on histology images using convolutional neural networks. IEEE Access:1–1. https://doi.org/10.1109/ACCESS.2018.2831280
Bayramoglu N, Kannala J, Heikkila J (2017) Deep learning for magnification independent breast cancer histopathology image classification. Paper presented at the Proceedings - International Conference on Pattern Recognition
Bejnordi BE, Zuidhof G, Balkenhol M, Hermsen M, Bult P, van Ginneken B, Karssemeijer N, Litjens G, van der Laak J (2017) Context-aware stacked convolutional neural networks for classification of breast carcinomas in whole-slide histopathology images. J Med Imaging 4(4):8. https://doi.org/10.1117/1.jmi.4.4.044504
Byun H, Lee S-W (2002) Applications of support vector machines for pattern recognition: a survey Pattern recognition with support vector machines. Springer, Berlin, pp 213–236
Carneiro G, Nascimento J, Bradley AP (2017) Automated analysis of unregistered multi-view mammograms with deep learning. IEEE Trans Med Imaging 36(11):2355–2365. https://doi.org/10.1109/TMI.2017.2751523
Chang J, Yu J, Han T, Chang HJ, Park E (2017) A method for classifying medical images using transfer learning: A pilot study on histopathology of breast cancer. Paper presented at the 2017 IEEE 19th international conference on e-health networking, Applications and Services (Healthcom)
Cireşan DC, Giusti A, Gambardella LM, Schmidhuber J (2013) Mitosis detection in breast cancer histology images with deep neural networks. Paper presented at the international conference on medical image computing and computer-assisted intervention
Elmore JG, Longton GM, Carney PA et al (2015) Diagnostic concordance among pathologists interpreting breast biopsy specimens. JAMA 313(11):1122–1132. https://doi.org/10.1001/jama.2015.1405
Evans AJ (2011) Re: barriers and facilitators to adoption of soft copy interpretation from the user perspective: lessons learned from filmless radiology for slideless pathology. J Pathol Inform 2: 1. Patterson et al Journal of Pathology Informatics 2
Feng Y, Zhang L, Yi Z (2018) Breast cancer cell nuclei classification in histopathology images using deep neural networks. Int J Comput Assist Radiol Surg 13(2):179–191. https://doi.org/10.1007/s11548-017-1663-9
Gandomkar Z, Brennan PC, Mello-Thoms C (2018) MuDeRN: multi-category classification of breast histopathological image using deep residual networks. Artif Intell Med. https://doi.org/10.1016/j.artmed.2018.04.005
Hadad O, Bakalo R, Ben-Ari R, Hashoul S, Amit G (2017) Classification of breast lesions using cross-modal deep learning. Paper presented at the proceedings - international symposium on biomedical imaging
Han S, Kang HK, Jeong JY, Park MH, Kim W, Bang WC, Seong YK (2017a) A deep learning framework for supporting the classification of breast lesions in ultrasound images. Phys Med Biol 62(19):7714–7728. https://doi.org/10.1088/1361-6560/aa82ec
Han Z, Wei B, Zheng Y, Yin Y, Li K, Li S (2017b) Breast cancer multi-classification from histopathological images with structured deep learning model. Sci Rep 7(1). https://doi.org/10.1038/s41598-017-04075-z
Jiang F, Liu H, Yu S, Xie Y (2017) Breast mass lesion classification in mammograms by transfer learning. Paper presented at the ACM international conference proceeding series
Khan AM, Rajpoot N, Treanor D, Magee D (2014) A nonlinear mapping approach to stain normalization in digital histopathology images using image-specific color deconvolution. IEEE Trans Biomed Eng 61(6):1729–1738
Kim DH, Kim ST, Ro YM (2016) Latent feature representation with 3-D multi-view deep convolutional neural network for bilateral analysis in digital breast tomosynthesis. Paper presented at the 2016 IEEE international conference on acoustics, speech and signal processing (ICASSP)
Kotsiantis SB, Zaharakis I, Pintelas P (2007) Supervised machine learning: a review of classification techniques. Emerging Artificial Intelligence Applications in Computer Engineering, 160:3–24.
Krizhevsky A, Sutskever I, Hinton GE (2012) Imagenet classification with deep convolutional neural networks. Paper presented at the Advances in neural information processing systems
Kumar I, Bhadauria HS, Virmani J, Thakur S (2017) A classification framework for prediction of breast density using an ensemble of neural network classifiers. Biocybern Biomed Eng 37(1):217–228. https://doi.org/10.1016/j.bbe.2017.01.001
Kuramochi M, Karypis G (2005) Gene classification using expression profiles: a feasibility study. Int J Artif Intell Tools 14(04):641–660
Macenko M, Niethammer M, Marron JS, Borland D, Woosley JT, Guan X, ... Thomas NE (2009) A method for normalizing histology slides for quantitative analysis. Paper presented at the Biomedical Imaging: From Nano to Macro, 2009. ISBI'09. IEEE international symposium on
Murtaza G, Shuib L, Wah TY, Mujtaba G, Mujtaba G (2018) Breast cancer classification from histopathology images using deep neural network. Paper presented at the data science research symposium 2018
Murtaza G, Shuib L, Abdul Wahab AW, Mujtaba G, Mujtaba G, Nweke HF, al-garadi MA, Zulfiqar F, Raza G, Azmi NA (2019a) Deep learning-based breast cancer classification through medical imaging modalities: state of the art and research challenges. Artif Intell Rev:1–66. https://doi.org/10.1007/s10462-019-09716-5
Murtaza G, Shuib L, Mujtaba G, Raza G (2019b) Breast cancer multi-classification through deep neural network and hierarchical classification approach. Multimed Tools Appl:1–31. https://doi.org/10.1007/s11042-019-7525-4
Nahid AA, Kong YA (2017) Local and global feature utilization for breast image classification by convolutional neural network. Paper presented at the 2017 international conference on digital image computing - techniques and applications, New York
Nahid AA, Kong Y (2018) Histopathological breast-image classification using local and frequency domains by convolutional neural network. Information (Switzerland) 9(1). https://doi.org/10.3390/info9010019
Nahid AA, Mehrabi MA, Kong Y (2018) Histopathological breast cancer image classification by deep neural network techniques guided by local clustering. BioMed Research International. https://doi.org/10.1155/2018/2362108
Nair V, Hinton GE (2010) Rectified linear units improve restricted boltzmann machines. Paper presented at the proceedings of the 27th international conference on machine learning (ICML-10)
Nascimento CDL, Silva SDS, da Silva TA, Pereira WCA, Costa MGF, Costa Filho CFF (2016) Breast tumor classification in ultrasound images using support vector machines and neural networks. Revista Brasileira de Engenharia Biomedica 32(3):283–292. https://doi.org/10.1590/2446-4740.04915
Nejad EM, Affendey LS, Latip RB, Ishak IB (2017) Classification of histopathology images of breast into benign and malignant using a single-layer convolutional neural network. Paper presented at the ACM international conference proceeding series
Rasti R, Teshnehlab M, Phung SL (2017) Breast cancer diagnosis in DCE-MRI using mixture ensemble of convolutional neural networks. Pattern Recogn 72:381–390. https://doi.org/10.1016/j.patcog.2017.08.004
Reinhard E, Adhikhmin M, Gooch B, Shirley P (2001) Color transfer between images. IEEE Comput Graph Appl 21(5):34–41
Rennie JD, Shih L, Teevan J, Karger DR (2003) Tackling the poor assumptions of naive bayes text classifiers. Paper presented at the proceedings of the 20th international conference on machine learning (ICML-03)
Rouhi R, Jafari M, Kasaei S, Keshavarzian P (2015) Benign and malignant breast tumors classification based on region growing and CNN segmentation. Expert Syst Appl 42(3):990–1002. https://doi.org/10.1016/j.eswa.2014.09.020
Samala RK, Chan HP, Hadjiiski LM, Helvie MA, Cha KH, Richter CD (2017) Multi-task transfer learning deep convolutional neural network: application to computer-aided diagnosis of breast cancer on mammograms. Phys Med Biol 62(23):8894–8908. https://doi.org/10.1088/1361-6560/aa93d4
Samala RK, Chan HP, Hadjiiski LM, Helvie MA, Richter C, Cha K (2018) Evolutionary pruning of transfer learned deep convolutional neural network for breast cancer diagnosis in digital breast tomosynthesis. Phys Med Biol 63(9):8. https://doi.org/10.1088/1361-6560/aabb5b
Spanhol FA, Oliveira LS, Petitjean C, Heutte L (2016a) Breast cancer histopathological image classification using convolutional neural networks. Paper presented at the proceedings of the international joint conference on neural networks
Spanhol FA, Oliveira LS, Petitjean C, Heutte L (2016b) A dataset for breast cancer histopathological image classification. IEEE Trans Biomed Eng 63(7):1455–1462
Spanhol FA, Oliveira LS, Cavalin PR, Petitjean C, Heutte L (2017) Deep features for breast cancer histopathological image classification. Paper presented at the systems, man, and cybernetics (SMC), 2017 IEEE international conference on
U.S. Department of Health and Human Services (2018) US Cancer Statistics Working Group U.S. Cancer Statistics Data Visualizations Tool
Wan T, Cao J, Chen J, Qin Z (2017) Automated grading of breast cancer histopathology using cascaded ensemble with combination of multi-level image features. Neurocomputing 229:34–44. https://doi.org/10.1016/j.neucom.2016.05.084
Wang H, Roa AC, Basavanhally AN, Gilmore HL, Shih N, Feldman M, … Madabhushi A (2014) Mitosis detection in breast cancer pathology images by combining handcrafted and convolutional neural network features. Journal of Medical Imaging 1(3):034003
Wolpert DH, Macready WG (1997) No free lunch theorems for optimization. IEEE Trans Evol Comput 1(1):67–82. https://doi.org/10.1109/4235.585893
Xu J, Luo X, Wang G, Gilmore H, Madabhushi A (2016) A deep convolutional neural network for segmenting and classifying epithelial and stromal regions in histopathological images. Neurocomputing 191:214–223. https://doi.org/10.1016/j.neucom.2016.01.034
Yosinski, J., Clune, J., Bengio, Y., & Lipson, H. (2014) How transferable are features in deep neural networks? Paper presented at the Advances in neural information processing systems
Zheng Y, Jiang Z, Xie F, Zhang H, Ma Y, Shi H, Zhao Y (2017) Feature extraction from histopathological images based on nucleus-guided convolutional neural network for breast lesion classification. Pattern Recogn 71:14–25. https://doi.org/10.1016/j.patcog.2017.05.010
Acknowledgements
This work was supported by University Malaya Research Grant Program – AFR (Frontier Science) [RG380-17AFR].
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Murtaza, G., Shuib, L., Wahab, A.W.A. et al. Ensembled deep convolution neural network-based breast cancer classification with misclassification reduction algorithms. Multimed Tools Appl 79, 18447–18479 (2020). https://doi.org/10.1007/s11042-020-08692-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11042-020-08692-1