Peerj 6201
Peerj 6201
ABSTRACT
It is important to detect breast cancer as early as possible. In this manuscript, a new
methodology for classifying breast cancer using deep learning and some segmentation
techniques are introduced. A new computer aided detection (CAD) system is proposed
for classifying benign and malignant mass tumors in breast mammography images. In
this CAD system, two segmentation approaches are used. The first approach involves
determining the region of interest (ROI) manually, while the second approach uses
the technique of threshold and region based. The deep convolutional neural network
(DCNN) is used for feature extraction. A well-known DCNN architecture named
AlexNet is used and is fine-tuned to classify two classes instead of 1,000 classes. The
last fully connected (fc) layer is connected to the support vector machine (SVM)
classifier to obtain better accuracy. The results are obtained using the following publicly
available datasets (1) the digital database for screening mammography (DDSM); and
(2) the Curated Breast Imaging Subset of DDSM (CBIS-DDSM). Training on a large
number of data gives high accuracy rate. Nevertheless, the biomedical datasets contain
a relatively small number of samples due to limited patient volume. Accordingly, data
augmentation is a method for increasing the size of the input data by generating new
data from the original input data. There are many forms for the data augmentation;
the one used here is the rotation. The accuracy of the new-trained DCNN architecture
is 71.01% when cropping the ROI manually from the mammogram. The highest area
Submitted 23 May 2018 under the curve (AUC) achieved was 0.88 (88%) for the samples obtained from both
Accepted 3 December 2018
Published 28 January 2019 segmentation techniques. Moreover, when using the samples obtained from the CBIS-
DDSM, the accuracy of the DCNN is increased to 73.6%. Consequently, the SVM
Corresponding author
Dina A. Ragab, [email protected] accuracy becomes 87.2% with an AUC equaling to 0.94 (94%). This is the highest AUC
value compared to previous work using the same conditions.
Academic editor
Jaume Bacardit
Additional Information and Subjects Data Mining and Machine Learning
Declarations can be found on
page 19 Keywords The deep convolutional neural network, The support vector machine, The computer
aided detection
DOI 10.7717/peerj.6201
Copyright
2019 Ragab et al. INTRODUCTION
Distributed under Breast cancer is one of the leading causes of death for women globally. According to the
Creative Commons CC-BY 4.0 World Health Organization (WHO), the number of cancer cases expected in 2025 will be
OPEN ACCESS
19.3 million cases. In Egypt, cancer is an increasing problem and especially breast cancer.
How to cite this article Ragab DA, Sharkas M, Marshall S, Ren J. 2019. Breast cancer detection using deep convolutional neural networks
and support vector machines. PeerJ 7:e6201 http://doi.org/10.7717/peerj.6201
Mammography is currently one of the important methods to detect breast cancer early.
The magnetic resonance imaging (MRI) is the most attractive alternative to mammogram.
However, the MRI test is done when the radiologists want to confirm about the existence of
the tumor. The drawback of the MRI is that the patient could develop an allergic reaction
to the contrasting agent, or that a skin infection could develop at the place of injection. It
may cause claustrophobia. Masses and microcalcifcations (MCs) are two important early
signs of the disease as shown in Fig. 1.
There are other indicators of breast cancer, such as architectural distortion (Bozek et al.,
2009) but these are less significant.
A mass can be either benign or malignant. The difference between benign and malignant
tumors is that the benign tumors have round or oval shapes, while malignant tumors have
a partially rounded shape with an irregular outline. In addition, the malignant mass will
appear whiter than any tissue surrounding it (Tang et al., 2009).
Recently, several researchers studied and proposed methods for breast mass classification
in mammography images. Sharkas, Al-Sharkawy & Ragab (2011) used the discrete wavelet
transform (DWT), the contourlet transform, and the principal component analysis (PCA)
methods for feature extraction. The system was able to detect and classify normal and
abnormal tissues. Additionally, it classified benign and malignant MC tumors. The
achieved rate was almost 98%. Ragab, Sharkas & Al-sharkawy (2013) used the DWT as
a feature extraction technique to detect mass abnormalities in the breast. In addition,
a comparison between support vector machines (SVM) and artificial neural networks
(ANN) for classifying normal, abnormal tissues, benign and malignant MCs tumors was
introduced. The achieved detection rate was 96% for ANN and 98% for SVM (Ragab,
Sharkas & Al-sharkawy, 2013). Cristina Juarez, Ponomaryov & Luis Sanchez (2006) applied
the functions db2, db4, db8 and db16 of the Daubechies wavelets family to detect MCs. The
achieved rate was close to 80% accuracy. Al-Sharkawy, Sharkas & Ragab (2012) detected
mass lesions using the DWT and SVM, the rate achieved was 92%. Suzuki et al. (2016) used
the deep convolutional neural network (DCNN) for mass detection. This study introduced
the transfer learning in the DCNN. The sensitivity achieved when differentiating between
mass and normal lesions was 89.9% using the digital database for screening mammography
(DDSM) (Heath et al., 2001). Their study was the first demonstration for the DCNN
mammographic CAD applications.
Dhungel, Carneiro & Bradley (2015) used the multi-scale belief network in detecting
masses in mammograms. The sensitivity achieved was 85%–90% using the INbreast and
DDSM-BCRP datasets, respectively. The main drawback of Dhungel, Carneiro & Bradley
(2015) is the limited size of the training set. The number of training and testing used
were 39 and 40 cases, respectively. Wichakam et al. (2016) used the DCNN and SVM. The
sensitivity achieved was 98.44% using the INbreast dataset. Arbach, Stolpen & Reinhardt
(2004) classified the MRI breast lesions using back propagation neural network (BPNN).
They found that the area under the receiver operating characteristics (ROC) curve was
0.913. Sahiner et al. (1996) used the convolutional neural network (CNN) to classify
normal and abnormal mass breast lesions. They used two segmentation techniques, the
first technique employed averaging and subsampling. The second technique employed
texture feature extraction methods applied to small sub-regions inside the ROI. The results
obtained were 90% true positive rate (TPR) and 31% false positive rate (FPR). Jain &
Levy (2016) used AlexNet to classify benign and malignant masses in mammograms of
the DDSM dataset (Heath et al., 2001) and the accuracy achieved was 66%. Huynh & Giger
(2016) used the DCNN features to classify benign and malignant tumors. The area under
the curve (AUC) reached 0.81. Jiang (2017) introduced a new dataset named BCDR-F03
(Film Mammography dataset number 3). They used the GoogLeNet and the AlexNet, to
classify breast lesions with an AUC of 0.88 and 0.83, respectively.
Zhu et al. (2017) proposed an end to end trained deep multi-instance networks for mass
classification based on the whole mammogram image and not the region of interest (ROI).
Moreover, the deep learning methods were mentioned in some papers for breast cancer
classification as in Dhungel, Carneiro & Bradley (2017a), Dhungel, Carneiro & Bradley
(2017b), Dhungel, Carneiro & Bradley (2016), and Ching et al. (2017).
METHODOLOGY
Generally, a CAD system consists of several steps as follows (1) image enhancement, (2)
image segmentation, (3) feature extraction, (4) feature classification, and finally, (5) an
evaluation for the classifier.
The novelty of this work is to extract the ROI using two techniques and replace the last
fully connected layer of the DCNN architecture with SVM. The proposed CAD system
used in this work is illustrated in Fig. 2. Each block is described in detail in the following
sub-sections.
Image enhancement
Image enhancement is processing the mammogram images to increase contrast and
suppress noise in order to aid radiologists in detecting the abnormalities.
There are many image enhancement techniques as in (Zabalza et al., 2015; Qiao et al.,
2017) among which is the adaptive contrast enhancement (AHE). The AHE is capable
of improving local contrast and bringing out more details in the image. It is an excellent
contrast enhancement method for both natural and medical images (Pizer et al., 1987) and
(Pisano et al., 1998). However, it can also produce significant noise.
In this manuscript, contrast-limited adaptive histogram equalization (CLAHE) which is
a type of AHE will be used to improve the contrast in images (Pizer et al., 1987) and (Pisano
et al., 1998).
One of the disadvantages of AHE is that it may over enhance the noise in the images due
to the integration operation. Therefore, the CLAHE is employed as it uses a clip level to
limit the local histogram in order to restrict the amount of contrast enhancement for each
pixel (Sahakyan & Sarukhanyan, 2012).
The CLAHE algorithm can be summarized as follows: (Sahakyan & Sarukhanyan, 2012).
1. Divide the original image into contextual regions of equal size,
2. Apply the histogram equalization on each region,
3. Limit this histogram by the clip level,
4. Redistribute the clipped amount among the histogram, and
5. Obtain the enhanced pixel value by the histogram integration.
An enhanced image using CLAHE and its histogram representation is shown in Fig. 3.
Image segmentation
Image segmentation is used to divide an image into parts having similar features and
properties. The main aim of segmentation is to simplify the image by presenting in an
easily analyzable way. Some of the most popular image segmentation methodologies are
edge, fuzzy theory, partial differential equation (PDE), artificial neural network (ANN),
threshold, and region-based segmentation (Kaur & Kaur, 2014).
Thresholding method
Thresholding methods are the simplest methods for image segmentation. The image pixels
are divided with respect to their intensity level. The most common type of thresholding
method is the global threshold (Kaur & Kaur, 2014). This is done by setting an appropriate
threshold value (T ). This value of (T ) will be constant for the whole image. On the basis
of (T ) the output image p(x,y) can be obtained from the original image q(x,y) as given in
Eq. (1),
(
1,ifq x,y > T
p x,y = (1)
0,ifq x,y < T
by the threshold and the region based method. The steps for the used method can be
summarized as follows:
1. Convert the original mammogram grayscale image into a binary image using the
threshold technique.
2. Binary image objects are labelled and the number of pixels are counted. All binary
objects are removed except for the largest one, which is the tumor with respect to the
threshold. The largest area is the area enclosed within the red contour labelled around
the tumor.
3. After the algorithm checks all pixels in the binary image, the largest area pixels within
the threshold are set to ‘‘1’’, otherwise all other pixels are set to ‘‘0’’.
4. The resulting binary image is multiplied with the original mammogram image to get
the final image without taking in consideration the rest of the breast region or any
other artifacts.
Feature extraction
There are many techniques for the feature extraction step. In recent years, deep
convolutional neural networks (DCNN) have attracted great attention due to their
outstanding performance. Consequently, in this manuscript the DCNN is used.
the ResNet (Sun, 2016), VGG16, and VGG 19. However, the most commonly used
architectures are the AlexNet, CiFarNet, and the Inception v1 (GoogleNet).
The AlexNet architecture achieved significantly better performance over the other
deep learning methods for ImageNet Large Scale Visual Recognition Challenge (ILSVRC)
2012. This success has revived the interest in CNNs in computer vision. AlexNet has five
convolution layers, three pooling layers, and two fully connected layers with approximately
60 million free parameters (Krizhevsky, Sutskever & Hinton, 2012). The AlexNet CNN
architecture is shown in Fig. 5.
The layers of conv1-5 in Fig. 5 are the convolution layers. Each neuron in the convolution
layers computes a dot product between their weights and the local region that is connected
to the input volume (Krizhevsky, Sutskever & Hinton, 2012).
The pooling layers are pool1, pool2, and pool5 as shown in Fig. 5. These layers perform
a down sampling operation along the spatial dimensions to reduce the amount of
computation and improve the robustness (Suzuki et al., 2016; Krizhevsky, Sutskever &
Hinton, 2012).
The layers of norm1-2 in Fig. 5 are the normalization layers. They perform a kind of
lateral inhibition that is observed in the brain (Krizhevsky, Sutskever & Hinton, 2012).
Additionally, the fully connected layers are fc6, fc7, and fc8 as shown in Fig. 5. Neurons
in the fully connected layer have full connections to all neurons in the previous layer, as
in ordinary feedforward neural networks (Krizhevsky, Sutskever & Hinton, 2012; Deng et
al., 2009).
Transfer learning
The DCNN is pre-trained firstly using the ImageNet dataset, which contains 1.2 million
natural images for classification of 1,000 classes. Then, the last fully connected layer is
replaced by a new layer for the classification of two classes; benign and malignant masses.
Figure 5 shows the fine-tuning of the AlexNet to classify only two classes (Deng et al., 2009).
To retrain the AlexNet after fine-tuning the fully connected layer to two classes, some
parameters must be set; the iteration number and the primary learning rate are set to 104
and 10−3 , respectively. Whereas, the momentum is set to 0.9 and the weight decay is set to
5×10−4 . These configurations are to ensure that the parameters are fine-tuned for medical
Classification
In this step, the ROI is classified as either benign or malignant according to the features.
There are lots of classifier techniques; such as linear discriminant analysis (LDA), artificial
neural networks (ANN), binary decision tree, and support vector machines (SVM).
In this manuscript, the SVM is used because it achieved high classification rates in the
breast cancer classification problem.
SVM is a machine learning algorithm that analyses data for classification and it is a
supervised learning method that sorts data in categories. The aim of SVM is to formulate a
computationally efficient way of learning by separating hyper planes in a high dimensional
feature space (Gunn, 1998).
There are many hyper-planes that could classify two data sets. The optimum hyper-plane
that should be chosen is the one with the maximum margin. The margin is defined as the
width by which the boundary could increase before hitting a data point. The support
vectors are considered the data points that the margin pushes up. Thus, the goal of the
SVM is to find the optimum hyper-plane that separates clusters of target vectors on the
opposing sides of the plane (El-naqa et al., 2002).
Evaluation
There are several evaluation tools to assess a classifier amongst them, is the confusion
matrix, the accuracy, the receiver-operating curve (ROC), the area under the ROC curve
(AUC), the precision, and the F1 score.
The accuracy
Accuracy is the measure of a correct prediction made by the classifier. It gives the ability of
performance of the whole classifier. The accuracy is defined as in Eq. (2).
TP + TN
accuracy = (2)
TN + FP + FN + TP
The Receiver operating characteristic (ROC)
The ROC analysis is a well-known evaluation method for detecting tasks. Firstly, a ROC
analysis was used in medical decision-making; consequently, it was used in medical
imaging.
The ROC curve is a graph of operating points which can be considered as a plotting of
the true positive rate (TPR) as a function of the false positive rate (FPR).
The TPR and the FPR are also called sensitivity (recall) and specificity, respectively. They
are defined as in Eqs. (3) and (4).
TP
sensitivity = (3)
TP + FN
TN
specificity = (4)
TN + FP
Precision
Precision is the ratio of correctly predicted positive observations to the total predicted
positive observations. High precision relates to the low FPR. The precision is calculated
using the following equation,
TP
Precision = (5)
TP + FP
F1 score
F1 score is the weighted average of precision and recall. It is used as a statistical measure
to rate the performance of the classifier. Therefore, this score takes both false positives and
false negatives into account. F1 score is defined as in Equation (6)
2 * Recall * Precision
F1 score = (6)
Recall + Precision
Experimental setup
The proposed DCNN based SVM classifier was applied to the mammogram images
providing the possibility of each image to belong to one of the two classes either benign or
malignant.
In this work, the most widely used DDSM mammogram dataset (Heath et al., 2001) has
been chosen to verify the proposed methods using MATLAB. The DDSM dataset consists
of 2,620 cases available in 43 volumes. The volumes could be normal, benign, or malignant
DCNN architecture
The Alexnet DCNN architecture is used in this manuscript after fine-tuning to classify two
classes instead of 1,000 classes. A conventional DCNN consists of a convolutional layer,
a pooling layer, and a fully connected (fc) layer. The DCNN architecture is formed by
stacking all these layers together. Figure 6 shows a complete description of each layer in
the AlexNet architecture.
In the convolutional layer number (1) as an example, the output of this layer is calculated
using Equation (7). The output is equals to 55 × 55 × 96, which indicates that the size of
the feature map is 55 × 55 in width and in height. In addition, the number of feature maps
is 96.
input − filter size
The output size of the conv layer = + 1. (7)
Stride
On the other hand, the output size of the pooling layer is calculated using Eq. (8).
output of conv − pool size
The output size of the pool layer = + 1. (8)
Stride
Data augmentation
Generally, training on a large number of training samples performs well and give high
accuracy rate. However, the biomedical datasets contain a relatively small number of
samples due to limited patient volume. Accordingly, data augmentation is a method for
increasing the size of the input data by generating new data from the original input data.
There are many strategies for data augmentation; the one used here in this manuscript is
the rotation. Each original image is rotated by 0, 90, 180, and 270 degrees. Therefore, each
image is augmented to four images.
RESULTS
DDSM Dataset
A subset from the DDSM was extracted to apply the proposed methods. Each sample
was augmented to four images. In this work 70% of images were used for training and
the remainder for testing. This is the common ratio used in the classification problem.
The number of training and testing samples for each segmentation technique is shown in
Table 2. All experiments were validated using five cross fold validation.
First, the samples were enhanced and segmented using the two methods mentioned in
‘Methodology’. Then the features were extracted using CNN. The samples went through
the SVM technique for classification.
Table 2 The number of training and testing samples for all the datasets used.
To train the AlexNet, the maximum number of Epochs was set to 20.
The input layer of the AlexNet architecture requires that the size of the image is
227 × 227 × 3. Therefore, there is a pre-processing step to convert all the input images
regardless of their sizes to the size required by the AlexNet.
When using the first segmentation technique the accuracy of the new-trained AlexNet
was only 71.01%. This was achieved when extracting and classifying the lesions with the
DCNN. Whereas, when attaching the DCNN to the SVM to obtain better result, the
accuracy with linear kernel function was 79% with AUC equals to 0.88 (88%). Figure 8
(A) and (B) demonstrate the SVM classification accuracy between benign and malignant
tumors samples and the ROC curve computed in this case.
Whereas, when using the second segmentation technique, the DCNN features accuracy
reached only 69.2%. However, the accuracy of the SVM classifier with linear kernel
function increased to 80.9% with AUC equals to 0.88 (88%). This is clear in Fig. 8C and in
the computed ROC curve shown in Fig. 8D.
A comparison between all the SVM kernels with all the scores calculated for the two
segmentation techniques are illustrated in Tables 3 and 4, respectively.
When calculating the sensitivity, specificity, precision, and F1 score for each SVM kernel
function for both segmentation techniques, it was proved that the kernel with highest
accuracy has all the other scores high as well.
Furthermore, the testing error for the first and second segmentation techniques was
30.17% and 30.43%, respectively.
Table 5 summarizes all the results obtained for the classification of benign and malignant
masses for both segmentation techniques for the DDSM dataset.
Table 3 The accuracy of SVM with different kernel functions for cropping the ROI manually for the
DDSM dataset. Numbers in red indicate the best values between the several techniques.
Table 5 The summary of the results obtained to classify benign and malignant masses for the DDSM
dataset. Numbers in red indicate the best values between the several techniques.
Segmentation techniques
Cropping ROI manually Threshold + Region based
Trained DCNN accuracy 71.01% 69.2%
Error in testing 30.17% 30.43%
SVM accuracy 79% 80.5%
Sensitivity 0.763 0.774
Specificity 0.822 0.842
AUC 0.88 0.88
Precision 0.84 0.86
F1 score 0.8 0.815
CBIS-DDSM Dataset
For this dataset, the samples were only enhanced and the features were extracted using the
DCNN. This is because that the samples of this dataset were already segmented.
Data augmentation was applied to all the mass samples in this dataset as well to increase
the training samples. The samples were augmented to four images using the rotation
technique. When using the DCNN for feature extraction and classification the accuracy
became 73.6%. Additionally, when classifying the features extracted from the DCNN using
the SVM the accuracy with medium Gaussian kernel function reached 87.2% as illustrated
in Table 6. The AUC was 0.94 (94%). The ROC curve is shown in Fig. 9.
By comparing to other researches results, either when using the AlexNet architecture
with or other DCNN architectures, the results of the new proposed methods achieved the
highest results. This is clear in Tables 7 and 8.
In Table 7, some of the previous work using the AlexNet architecture is shown. On the
other hand, Table 8 shows a comparative view of several mass detection methods based on
DCNN, including the newly proposed method.
DISCUSSIONS
This work presented a new approach for classifying breast cancer tumors. It introduced
a new CAD system including two approaches for segmentation techniques. The first one
Table 6 Different evaluation scores calculated for SVM with different kernel functions for the CBIS-
DDSM dataset. Numbers in red indicate the best values between the several techniques.
was cropping the ROI manually using circular contours from the DDSM dataset that was
already labelled in the dataset. The second one depends on the threshold and region based
techniques, the threshold was determined using the red contour surrounding the tumor
area.
These two segmentation techniques were only applied on the DDSM dataset. However,
for the CBIS-DDSM dataset the data provided was already segmented so therefore, no need
for the segmentation step.
The features were extracted using the DCNN and especially the pre-trained architecture
AlexNet. The transfer learning technique was presented by replacing the last fully connected
layer with a new layer to differentiate between two classes; benign and malignant rather
than 1,000 classes. The features went through the DCNN and SVM for classification, in
which the last fully connected layer was connected to SVM to obtain better results.
Table 8 A comparative view of several mass detection methods based on different DCNN architectures and datasets, including the newly pro-
posed method. Numbers in red indicate the best values between the several techniques.
To increase the number of training samples to improve the accuracy data augmentation
was applied to the samples in which all the samples were rotated by four angles 0, 90, 180,
and 270 degrees. This is demonstrated in Table 2.
For the DDSM samples, when using the DCNN as a classifier the accuracy of the
new-trained architecture for the first segmentation method was higher than that of the
second method. It recorded to be 71.01%.
For the DDSM samples when cropping the ROI manually, it is obvious from Table 3
that the SVM with linear kernel function achieved the highest values compared to the other
kernels. The linear SVM achieved an accuracy of 79%and AUC, 0.88 (88%). Moreover, the
sensitivity, specificity, precision, and F1 score reached 0.763 (76.3%), 0.822 (82.22%), 0.85
CONCLUSIONS
The goal of this work was to detect the masses and to classify benign and malignant tissues
in mammograms.
A new CAD system was proposed. Two segmentation techniques were suggested. In
the first technique, the ROI was cropped manually from the original image using circular
contours. This was because the tumors in the DDSM dataset were labelled with a red
contour.
Whereas, in the second technique, the region based method was used by setting a
threshold, which was found to be equal to 76, and determining the largest area including
this threshold.
In the feature extraction step, the DCNN was used. The AlexNet was retrained to
distinguish between two classes and its parameters were changed to classify medical
images.
The accuracy of the DCNN of the first segmentation method was higher than that of the
second method by 1.8% using the DDSM dataset.
To achieve better accuracy, the last fully connected layer in the DCNN was replaced by
the SVM.
When comparing between the two segmentation techniques for the DDSM dataset it
was found that the SVM with linear kernel function for the second segmentation technique
provided promising results. The accuracy, AUC, sensitivity, specificity, precision, and F1
score achieved 80.5%, 0.88 (88%), 0.774 (77.4%), 0.842 (84.2%), 0.86 (86%), and 0.815
(81.5%), respectively.
Moreover, when using the samples extracted from the CBIS-DDSM dataset, the accuracy
of the DCNN increased to 73.6%. In addition the accuracy of the SVM with medium
Gaussian kernel function became 87.2% with AUC reaching 0.94 (94%). Furthermore, the
sensitivity, specificity, precision, and F1 score reached 0.862 (86.2%), 0.877 (87.7%), 0.88
(88%), and 0.871 (87.1%), respectively.
The proposed CAD system could be used to detect the other abnormalities in the breast
such as MCs.
For future work, other networks will be suggested which include the very deep
convolutional network (VGG) and the residual (ResNet) architecture.
Funding
The authors received no funding for this work.
Author Contributions
• Dina A. Ragab conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, prepared figures and/or
tables, authored or reviewed drafts of the paper, approved the final draft, suggested to
segment the tumor with 2 new ways.
• Maha Sharkas conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, prepared figures and/or
tables, authored or reviewed drafts of the paper, approved the final draft, suggested to
DCNN-based SVM.
• Stephen Marshall and Jinchang Ren conceived and designed the experiments, authored
or reviewed drafts of the paper, approved the final draft.
Data Availability
The following information was supplied regarding data availability:
The results are obtained using the following publicly available datasets (1) the digital
database for screening mammography (DDSM); and (2) the Curated Breast Imaging Subset
of DDSM (CBIS-DDSM):
http://marathon.csee.usf.edu/Mammography/Database.html
https://wiki.cancerimagingarchive.net/display/Public/CBIS-DDSM.
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