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31 May 2022

Classifying Breast Density from Mammogram with Pretrained CNNs and Weighted Average Ensembles

,
,
and
1
Department of Computer Science, Faculty of Computing and Information Technology, King Abdulaziz University, Jeddah 22254, Saudi Arabia
2
Consultant Radiologist, King Abdulaziz Medical City, Jeddah 11426, Saudi Arabia
*
Author to whom correspondence should be addressed.
Appl. Sci.2022, 12(11), 5599;https://doi.org/10.3390/app12115599
This article belongs to the Topic Artificial Intelligence in Healthcare
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Abstract

We are currently experiencing a revolution in data production and artificial intelligence (AI) applications. Data are produced much faster than they can be consumed. Thus, there is an urgent need to develop AI algorithms for all aspects of modern life. Furthermore, the medical field is a fertile field in which to apply AI techniques. Breast cancer is one of the most common cancers and a leading cause of death around the world. Early detection is critical to treating the disease effectively. Breast density plays a significant role in determining the likelihood and risk of breast cancer. Breast density describes the amount of fibrous and glandular tissue compared with the amount of fatty tissue in the breast. Breast density is categorized using a system called the ACR BI-RADS. The ACR assigns breast density to one of four classes. In class A, breasts are almost entirely fatty. In class B, scattered areas of fibroglandular density appear in the breasts. In class C, the breasts are heterogeneously dense. In class D, the breasts are extremely dense. This paper applies pre-trained Convolutional Neural Network (CNN) on a local mammogram dataset to classify breast density. Several transfer learning models were tested on a dataset consisting of more than 800 mammogram screenings from King Abdulaziz Medical City (KAMC). Inception V3, EfficientNet 2B0, and Xception gave the highest accuracy for both four- and two-class classification. To enhance the accuracy of density classification, we applied weighted average ensembles, and performance was visibly improved. The overall accuracy of ACR classification with weighted average ensembles was 78.11%.

1. Introduction

Artificial intelligence (AI) algorithms have improved and affected every aspect of modern life. In the last two decades, machine learning techniques and computer power have experienced momentous development, leading to an enormous increase in digital data in different fields. These advances have enabled researchers to solve real-world problems in many areas, including the medical image analysis field. Medical imaging was first used in 1895 [1]. Since that time, the devices and quality of medical imaging have continued to evolve. Today, medical imaging is an essential tool for diagnosing and detecting diseases such as cancer [2]. Cancer is a significant public health concern that affects people around the world, and it is the second leading cause of death in the US [3]. Breast cancer is one of the most prevalent cancers that affect women [4], but it can also arise in men [5]. In Saudi Arabia, in 2018, breast cancer was the most common type of cancer, with an incidence rate of 14.8% and a mortality rate of 8.5% [6]. In 2020, breast cancer remained the most common type of cancer in Saudi Arabia. Breast cancer is a disease caused by the abnormal growth of breast cells. Usually, somatic cells divide to produce new cells in an orderly manner. When the cells of a specific part of the body grow and divide out of control, a mass of tissue called a tumor is created. A tumor that consists of normal cells is benign. When the cells are abnormal and exhibit irregular behavior, it is a malignant or cancerous tumor [7]. Three distinct types of medical imaging are used to diagnose breast cancer. These are mammograms, ultrasound, and magnetic resonance imaging (MRI) [8]. Among the breast imaging techniques, the mammogram is considered the gold standard for detecting and diagnosis [9,10]. A mammogram is a type of medical imaging that uses a low-dose x-ray system to see inside the tissues of the breast [11]. There are two mammogram imaging modalities: digital and screen-film mammography. Screen-film mammography (SFM) consists of conventional analog mammographic films. SFM often contains various background objects, such as labels and markers, that need to be removed. Digital mammograms are also referred to as FFDM images; FFDM stands for full-field digital mammography. FFDM is the approved version in hospitals today [11]. Moreover, mammogram images can be found in several formats, including LJPG, DICOM, PGM, and TIFF. In the standard view for each breast, two X-ray images must be taken on both sides. Therefore, four images of both breasts must be examined. These four images are called: LEFT_CC, LEFT_MLO, RIGHT_CC, RIGHT_MLO [12,13]. The craniocaudal (CC) view is taken from above a horizontally compressed breast (head-to-foot picture). The CC view captures the medial portion and as much of the breast’s outer lateral region as possible. MedioLateralOblique (MLO) view captures the entire breast and often includes the lymph nodes and the pectoral muscle. Figure 1a,b show examples of the CC and MLO views, and Figure 2 illustrates the angle of each view [14]. Among the breast imaging techniques, the mammogram is considered the gold standard [9,10].
Figure 1. FFDM view for right breast.
Figure 2. The difference between CC and MLO views.

1.1. Breast Density

Breast density describes the amount of fibrous and glandular tissue in a breast compared with the amount of fatty tissue. The breast density is assigned to one of four classes in the mammogram report based on the ACR BI-RADS standard. In class A, the breasts are almost entirely fatty. A few areas of dense tissue scattered within the breasts indicate class B. In class C, the breasts are heterogeneously dense. Finally, in class D, breasts are extremely dense [8,15]. Breast density plays a significant role in detecting breast cancer and on the risk of developing breast cancer. The clinicians must identify breast density from a mammogram for each patient and write it in their reports. Usually, dense breasts—i.e., breasts categorized into class C or D—are more likely to be affected by breast cancer [16]. In [17], the authors studied the relationship between mammographic densities and breast cancer risk. The results showed that the ratio of positive cancer cases for the different ACR classes were as follows: D (13.7%), C (3.3%), B (2.7%), and A (2.2%). Table 1 illustrates the difference between ACR classes.
Table 1. Breast density classes.
Breast density is important and must be specified in breast screening medical reports. Determining breast density can be challenging and mostly subjective, especially if they have been affected by treatment such as chemotherapy [18].

1.2. Convolutional Neural Network (CNN)

CNNs are a type of artificial neural network usually used for classification and computer vision tasks. Therefore, CNNs are considered efficient tools for medical imaging classification. In addition to input and output layers, CNNs include three main types of layers: convolutional, pooling, and fully connected. The convolutional layer is the main part of the CNN; it incorporates input data, a filter, and a feature map. The pooling layer or down-sampling layer seeks to reduce the number of parameters in the input. In the fully connected layer, a neuron applies a linear transformation to the input vector through a weight matrix [19]. Figure 3 illustrates the general structure of the CNN, assuming an input image size is 28 by 28, and a target task is classifying images into one of 10 classes [20].
Figure 3. The general structure of a CNN.
The CNN model is affected by many factors, including the number of layers, layer parameters, and other hyperparameters of the model, such as the optimizer and loss function. The loss function is used to calculate the difference between the predicted value and the actual value. An optimizer is a function that modifies the weights and learning rate of the DL model to reduce the loss value and increase accuracy. With classification problems, especially when there are more than two classes, the categorical_crossentropy function is the best choice to calculate loss value [21]. Root mean square propagation (RMSProp), and adaptive moment estimation(Adam), are the most commonly used optimizers [22,23].

1.3. Transfer Learning and Pre-Trained CNNs

Transfer learning reuses the knowledge gained from a previous task in a new deep learning model. Usually, deep learning requires a large amount of data to achieve good results. However, it is often difficult to gather enough data, especially in the medical field. Therefore, transfer learning enhances the learning process when the dataset has limited samples [24]. A pre-trained model is a model that was created and trained to solve a problem that is related to the target task. For example, in image classification tasks, such as flower image classification, we can use VGG19, which is a pre-trained CNN used to classify images that was trained on a huge image dataset called ImageNet [25]. Table 2, presents the main information about the pre-trained CNN that was used in this paper [26,27]. This information includes the model name, the number of layers, the top-1 accuracy of the model in classifying ImageNet data, and the year the model was established. The top-1 accuracy checks if the class with the highest probability is the same as the target label [28]. All of the models were trained on ImageNet. The ImageNet is a large dataset of 14,197,122 annotated images belonging to more than 1000 categories [29].
Table 2. Pre-trained CNNs.
Many studies on applying machine learning and deep learning to classify breast density from mammogram have been conducted. However, we could not find a study that used local data from Saudi Arabia. Moreover, according to [30,31], breast density and ethnicity are associated. Therefore, an automated model to classify breast density trained on local mammogram datasets would be valuable. The main contribution of this paper is developing a breast density classification model that is suited for the local population in Saudi Arabia. The model is based on pre-trained CNNs and weighted average ensembles and applied to the KAMC dataset. The rest of this paper is divided as following, Section 2 explores recent related works that classify breast density from mammogram using deep learning techniques. Section 3 outlines our methodology. Section 4 presents and discusses our results. Finally, a conclusion is offered in Section 5.

3. Methodology

In this paper, we developed a model to classify breast density from mammograms based on pre-trained CNNs and weighted average ensembles. The key steps of our methodology are illustrate in Figure 4. The first stage entailed collecting the dataset from KAMC. Next, we prepared the data. Then, several pre-trained models were applied to classify breast density. Finally, a weighted average ensemble was employed to enhance the CNN performance. Below, we describe each of the steps in sequence.
Figure 4. Methodology.

3.1. Dataset

The dataset was collected from King Abdulaziz Medical City, and it consists of 879 mammogram screenings taken between 1 January 2020 and 12 January 2021. The data collection took around three months, from 3 December 2020 to 28 February 2021, because the system allows only one record to be downloaded at a time, and we could not access the system when the radiologists were using it. Each case is associated with a medical report written by a radiologist. Patients’ private information, such as their names and IDs, was hidden from the reports. Only data that relates to the research and statistics were included. These data include the diagnosis, BI-RADS stage, ACR class, age, and gender. Most of the screenings were diagnosed as BI-RADS 2, but the data include all BI-RADS categories. As each screening included two or more images, there were 3083 images in total. The majority of cases were for women, with just a few cases for men. Figure 5 shows the gender distribution.
Figure 5. Gender distribution.
The dataset includes people between the ages of 28 and 89. The majority were above 40 years. Patients younger than 40 years of age had their mammograms done for specified indications. Figure 6 shows the age distribution chart. The four density classes in the ACR standard are represented in this dataset: 36.9% of the cases are in class B, 34.9% in class C, 21.6% in class A, and 6.6% in class D. This follows the normal distribution of ACR classes in other mammogram datasets; where class B is the majority class, there are more samples in class C than in class A, and class D is the minority class [38,48]. The chart in Figure 7 illustrates this distribution.
Figure 6. Age distribution.
Figure 7. ACR distribution.

3.2. Data Preparation

At this stage, we cleaned the data by removing mislabeled cases. The dataset was divided as follows: 80% was used for training and validation and 20% was used for testing with a fixed seed number. The images were converted into PNG format; the original image size was 4096 by 3328 pixels in RGB color mode. Converting images to PNG format does not compromise image quality through compression. Moreover, PNG format supports a wide color range. The images were then resized to 300 by 300 pixels, as their original size was too large to use during training. Finally, several augmentation techniques were applied, including horizontal flip, rotation, and translation, as in most of the related works.

3.3. Pre-Trained Model

We applied several pre-trained CNN models used in related works to classify breast density. These models were ResNet, Inception, DensNet, and VGG16 [34,36,37,44,47]. Moreover, we applied models based on VGG19, InceptionResNetV2, EfficientNetV2, and Xception. The models were applied to the entire dataset, without excluding cases that were affected by treatment. The structure of our proposed model is shown in Figure 8. First, the pre-trained CNN is loaded. Then a flatten layer is applied. After that, the model going through several dense and dropout layers. Finally, the output layer gives the density class.
Figure 8. Structure of the model.

3.4. Average Ensembles

Ensembles is a technique that applies machine learning and deep learning to enhance performance. Basically, ensembles combine multiple models instead of using just a single model. How these models are combined determines the type of ensembles technique used, which include stacking, bagging, boosting, and averaging. In stacking ensembles, a meta-learning model integrates the outputs of basic models that were trained on the entire training set. In contrast, the bagging technique trains many models separately on a subset of data before combining their predictions to generate an ensemble predictor. Boosting, meanwhile, uses sequential training, enabling subsequent models to focus on previously misclassified samples. Finally, in averaging ensembles, several models are trained on the training set, and during testing, the average of their predictions is taken. A subtype of averaging ensembles is weighted average ensembles. In a weighted average ensemble, each model is weighted according to certain criteria or based on a grid search. The final result is obtained through a dot product of the weight vector and the model predictions vector; after that, the sum or highest probable class is taking [49,50].
In our model, after we trained several pre-trained CNNs, we applied averaging ensembles to the CNNs. A grid search was applied to find the optimal weight for each model, and then weighted average ensembles were employed. Figure 9 and Figure 10 illustrate the idea of average and weighted average ensembles.
Figure 9. Average ensembles.
Figure 10. Weighted average ensembles.

3.5. Experimental Tools

We used the Tensorflow Keras library and the training was conducted on Google Colab Pro+. The loss function was categorical cross-entropy loss, and the optimizer was RMSprop with a learning rate of 0.0001. We used 100 epochs. The hyperparameters were chosen based on related works and a wide range of experiments. The dataset was divided, with 80% for training and validation and 20% for testing. A fixed seed number was used during data splitting to ensure that the data were divided in the same way each time and that splitting would not affect the testing of other hyperparameters. The performance was measured with accuracy and F1 scores, in addition to monitoring the confusion matrix and F1 of each class.

4. Results and Discussion

The experiments were started with applying pre-trained CNN models that used in the related works. Then, we investigated and tested recent and efficient pre-trained CNNs supported by Keras. These models included VGG19, InceptionResNetV2, EfficientNetV2, and Xception. Some models required a significant amount of memory, such as NasNet; therefore, we could not use them. The training/validation behavior based on accuracy and loss for each model is illustrated in Figure 11, Figure 12, Figure 13, Figure 14, Figure 15, Figure 16, Figure 17, Figure 18 and Figure 19. Moreover, Table 4, Table 5, Table 6, Table 7, Table 8, Table 9, Table 10, Table 11 and Table 12 report the performance of each model. Figure 11 explaining the behavior of the DenseNet based model. It can be notice that, the validation loss increase in oscillatory manner after epoch 40. The performance of DenseNet model, was low in terms of overall accuracy and F1 of each class, as shown in Table 4. Moreover, MobileNet model was the worst model in classifying breast density. We can notice this from training behavior in Figure 12, and testing results in Table 5. The loss value of ResNet50, increasing dramatically after epoch 80, as shown in Figure 13. Both ResNet50 and InceptionV3, have overall accuracy exceed 70%. However, the F1 of each class was better with ResNet50 model comparing with InceptionV3, as shown in Table 6 and Table 7. The training behaviors of VGG16 and VGG19, are very oscillate as illustrated in Figure 15 and Figure 16. Meanwhile, the performance of VGG16 and VGG19 shown in Table 8 and Table 9 were low, the overall accuracy and F1 score were under 65%. Comparing with ResNet50 and Inception V3, the InceptionResNetV2 model was worse, the behavior of the model and its performance present in Figure 17 and Table 10. The training behavior of the model based on Xception is shown in Figure 18, and the model’s performance illustrated in Table 11. Finally, the training behavior and testing performance of EfficientNetV2 is shown in Figure 19 and Table 12, respectively.
Figure 11. The training behavior of the model based on DenseNet121.
Figure 12. The training behavior of the model based on MobileNet.
Figure 13. The training behavior of the model based on ResNet50.
Figure 14. The training behavior of the model based on InceptionV3.
Figure 15. The training behavior of the model based on VGG16.
Figure 16. The training behavior of the model based on VGG19.
Figure 17. The training behavior of the model based on InceptionResNetV2.
Figure 18. The training behavior of the model based on Xception.
Figure 19. The training behavior of the model based on EfficientNetV2B0.
Table 4. DensNet 121.
Table 5. MobileNet.
Table 6. ResNet50.
Table 7. Inception V3.
Table 8. VGG16.
Table 9. VGG19.
Table 10. InceptionResNetV2.
Table 11. Xception.
Table 12. EfficientNetV2.
Our target was to classify breast density according to ACR standards. However, fatty and dense (or superclass) classifications were also performed. Table 13 and Table 14 summarize the accuracy and F1 scores of each model for ACR and superclass classification, respectively.
Table 13. ACR classification.
Table 14. Superclass classification.
We noticed, from monitoring the performance of each model, that some models performed better with specific classes. For example, InceptionV3 gave the highest F1 for class A, whereas ResNet50 gave the highest F1 for class C. The model based on Xception achieved the overall highest F1 score for class D. Therefore, average and weighted average ensembles were applied to reap the benefits of all models. Table 15 shows the performance of the average ensembles of all models. The overall accuracy of the proposed model with average ensembles was 74.7%. Furthermore, weighted average ensembles with grid search were applied. These reference exampling the idea of grid search [51] and how to apply it with average ensembles [52]. First, we applied weighted averages using the best five models, achieving an accuracy of 77.9%. Next, we selected the best four models, InceptionV3, ResNet50, EfficientNet, and Xception, resulting in an overall accuracy of 78.11%. Finally, we tried weighted average ensembles with the three best models, achieving an accuracy of 75.8%. More details on the weighted average ensemble performance are provided in Table 16, Table 17 and Table 18. A summary of the average and weighted average of ACR and superclass classification is provided in Table 19 and Table 20, respectively.
Table 15. Average ensembles.
Table 16. Weighted average ensembles with best 5 models.
Table 17. Weighted average ensembles with best 4 models.
Table 18. Weighted average ensembles with best 3 models.
Table 19. Ensembles for ACR classification.
Table 20. Ensembles for superclass classification.

5. Conclusions

Breast density describes the amount of fibrous and glandular tissue in a breast compared with the amount of fatty tissue. Breast density plays a significant role in detecting breast cancer and on the risk of developing breast cancer. Dense breasts are more likely to be affected by breast cancer. The Breast Imaging-Reporting and Data System (BI-RADS) is an assessment standard for reporting the breast cancer risk based on a mammogram image. It sorts breast density into one of four ACR classes. In class A, breasts are almost entirely fatty. A few areas of dense tissue are scattered within the breasts in class B. In class C, the breasts are heterogeneously dense. Finally, in class D, the breasts are extremely dense. In this paper, a breast density classification model from mammograms was developed. The model is based on pre-trained CNNs and weighted average ensembles. The dataset was collected from King Abdulaziz Medical City under the supervision of the King Abdullah International Medical Research Center (KAIMRC). The dataset consists of 879 mammogram screenings. Several model pre-trained convolutional neural networks were applied, including ResNet, Inception, DensNet, vgg16, vgg19, InceptionResNetV2, EfficientNetV2, and Xception. Among these models, InceptionV3, EfficientNet 2B0, and Xception gave the highest accuracy in both four- and two-class classification. We noticed from monitoring the performance of each model that some models performed better with specific classes. Therefore, average and weighted average ensembles were applied to reap the benefits of all models. After applying weighted average ensembles, the performance was improved noticeably. The overall accuracy of ACR classification with weighted average ensembles was 78.11%. For future works we recommend the following: different ensembles techniques, such as boosting ensembles, could be investigated; increasing the size of the dataset; and applying unsupervised learning segmentation techniques to segment ROIs.

Author Contributions

Conceptualization, E.J., G.A., N.A. and A.A.; methodology, E.J. and A.A.; software, E.J.; validation, E.J.; formal analysis, E.J.; investigation, E.J.; resources, N.A.; data curation, E.J. and N.A.; writing—original draft preparation, E.J.; writing—review and editing, E.J. and N.A.; visualization, E.J.; supervision, G.A. and A.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

We got the ethical approval to collect this dataset and perform the study from King Abdullah International Medical Research Center (KAIMRC). The KAIMRC is the research center of King Abdulaziz medical city in Jeddah.

Acknowledgments

We would like to acknowledge King Abdullah International Medical Research Center and King Abdulaziz Medical City radiology breast radiology section. They helped us collect the dataset and were very supportive.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript:
AIArtificial Intelligence
BI-RADSBreast imaging-reporting and data system
CNNConvolutional neural network
DICOMDigital image communication in medicine
KAMCKing Abdulaziz Medical City
RMS propRoot mean square propagation

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