Computers in Biology and Medicine 135 (2021) 104553

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Computers in Biology and Medicine

journal homepage: www.elsevier.com/locate/compbiomed

A hybrid methodology for breast screening and cancer diagnosis

using thermography☆
Roger Resmini a, b, Lincoln Faria da Silva d, *, Petrucio R.T. Medeiros c, Adriel S. Araujo b,
Débora C. Muchaluat-Saade c, Aura Conci b
a
Institute of Exact and Natural Sciences, Federal University of Rondonópolis, Cidade Universitária, Rondonópolis, MT, 78736-900, Brazil
b
Visual Lab, Institute of Computing, Fluminense Federal University, Av. Gal. Milton Tavares de Souza, S/N - Niterói, RJ, 24210-346, Brazil
c
Mídiacom Lab, Institute of Computing, Fluminense Federal University, R. Passo da Pátria 156, Niterói, RJ, 24210-240, Brazil
d
Advanced Research Medical Laboratory, Departament of Information Technology and Education in Health, Faculty of Medical Sciences, State University of Rio de
Janeiro, R. Professor Manuel de Abreu, 444, Rio de Janeiro, RJ, 20550-170, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: Breast cancer is the second most common cancer in the world. Early diagnosis and treatment increase the pa­
Breast cancer tient’s chances of healing. The temperature of cancerous tissues is generally different from that of healthy
Screening neighboring tissues, making thermography an option to be considered in the fight against cancer because it does
Diagnosis
not use ionizing radiation, venous access, or any other invasive process, presenting no damage or risk to the
Thermography
Texture
patient. In this paper, we propose a hybrid computational method using the Dynamic Infrared Thermography
GLCM (DIT) and Static Infrared Thermography (SIT) for abnormality screening and diagnosis of malignant tumor
(cancer), applying supervised and unsupervised machine learning techniques. We use the area under receiver
operating characteristic curve, sensitivity, specificity, and accuracy as performance measures to compare the
hybrid methodology with previous work in the literature. The K-Star classifier achieved accuracy of 99% in the
screening phase using DIT images. The Support Vector Machines (SVM) classifier applied on SIT images yielded
accuracy of 95% in the diagnosis of cancer. The results confirm the potential of the proposed approaches for
screening and diagnosis of breast cancer.

1. Introduction
Worldwide, 684,996 females died of breast cancer in 2020, and
768,646 deaths of women are predicted for 2025, according to the
World Health Organization (WHO) [83]. High breast cancer mortality
rates can be related to late cancer diagnosis. However, when breast
cancer is identified and treated in its early stages, the success of medical
care increases considerably. Moreover, treatment prognosis is inversely
proportional to tumor size and degree of tissue invasions [23].
Mammography is considered as gold standard for cancer early
detection. However, mammography has some limitations, such as high
false positive rates, insufficient effectiveness for dense breasts and use of
ionizing radiation. According to Arabi et al. [8], the risk of patients
developing breast cancer increases 2% for each X-ray exposure. Breast
infrared thermography is an exam that detects and records the infrared
radiation emitted by the breast surface. Thermography does not use
ionizing radiation, venous access, or any other invasive process, it does
not present any damage or risk to the patient. Infrared Thermography
(IT) is a functional exam providing physiological information on normal
or abnormal functioning of vascular, sensory and sympathetic nervous
systems, as well as inflammatory processes [6,34,63], in addition IT has
an extremely low cost when compared to other exams. There are two IT
modalities: Dynamic Infrared Thermography (DIT) and Static Infrared
Thermography (SIT) [36].
DIT is a method for monitoring the dynamic response of the skin
temperature after thermal stress. The most common thermal stress is
cooling using an electric fan, where the airflow is directed to the breast
[14]. Blood vessels produced by tumors usually do not have nervous
termination like embryological vessels. These vessels are endothelial
tubes, and do not respond to sympathetic stimulus. This way, the region

This work is the result of research projects funded by the CAPES, CNPq and FAPERJ government agencies and CAPES PRINT Project.
☆

* Corresponding author.
E-mail addresses: roger@ufr.edu.br (R. Resmini), lincoln@lampada.uerj.br, lincoln@lampada.uerj.br (L. Faria da Silva), petruciomedeiros@id.uff.br
(P.R.T. Medeiros), adrielsantos@id.uff.br (A.S. Araujo), debora@midiacom.uff.br (D.C. Muchaluat-Saade), aconci@ic.uff.br (A. Conci).

https://doi.org/10.1016/j.compbiomed.2021.104553
Received 15 December 2020; Received in revised form 2 May 2021; Accepted 2 June 2021
Available online 26 June 2021
0010-4825/© 2021 Elsevier Ltd. All rights reserved.
R. Resmini et al.
with tumor remains virtually unchanged when the breast is cooled. By
reducing the vascular diameter, healthy regions of the breast showed a
decrease of skin temperature more intense than the tumor regions of the
breast. Such characteristic can be observed by DIT exams [5,7,62,72].
SIT records the temperature distribution on the skin surface, and
does not consider its variation over time. SIT requires rigid environ­
mental conditions and more time for acclimatization of the patient to
examining room [36]. Previous recommendations are done to the pa­
tient in order to avoid changes in skin temperature and, consequently,
inconsistent thermal data of the analyzed area [6,66].
In this paper, we propose a computational methodology for breast
analysis by IT to screen patients (i.e. detect any abnormalities in the
breast) using DIT and diagnosis of malignant tumor (cancer) using SIT,
which characterizes it as hybrid. This work is an extension of Silva et al.
[68], where some aspects of the screening approach here discussed have
been presented, but despite that, a greater part of the manuscript is
completely new using SIT for diagnosis of malignant tumor (cancer).
In the remainder of this paper, Section 2 summarizes some important
related work emphasizing their characteristics. The database, the
acquisition protocols, and other important information are presented in
Section 3. Section 4 details the proposed hybrid methodology for
screening and diagnosis of breast cancer, which is the core and main
contribution of this work. Section 5 considers experimental analysis and
comparison with other work. Finally, in Section 6 conclusions and future
work are presented.
2. Related work
Borchartt et al. [14] showed a comprehensive survey on breast
thermography and corresponding taxonomy. A recent and complete
review about thermography using computational techniques with arti­
ficial intelligence is the work of Husaini et al. [40]. That work highlights
the contributions and drawbacks of each reported paper. Moreover it
proposes open issues for future research in the area. Etehadtavakol et al.
[20], Jakubowska et al. [43], Tan et al. [75] and Heidari et al. [35]
presented major research achievements in medical IT, associating it to
the possibility of early breast cancer detecting using SIT images. In
contrast, we propose in this paper a hybrid methodology that analyzes
breast images generated by both DIT and SIT.
Arora et al. [10] evaluated the thermal asymmetry between breasts
after performing cooling of breast region, in order to seek areas with the
greatest difference in temperature when compared to surrounding areas.
The outputs are color images where suspicious regions are marked.
Their computational method based on artificial neural network achieved
sensitivity of 97%, specificity of 27% and negative predictive value of
82%.
Wishart et al. [84] used temperature differences and thermal sym­
metry measures to detect patients with breast cancer. Areas of the breast
that exhibit abnormal cooling patterns received a color coding. By using
artificial intelligence techniques, the authors achieved sensitivity of
70% and specificity of 48%.
Gerasimova et al. [25] performed a multifractal analysis over DIT
breast temperature time series, in order to detect differences between
tissue with malignant tumor and healthy tissue. The modulus maxima
wavelet transform method was performed to characterize multifractal
properties of 1D time series of cancerous and healthy breasts. The au­
thors noticed that complex scalar multifractal properties over autonomic
regulation series were drastically altered in cancerous breasts. A total of
30,000 image frames were acquired during 10 min. The authors used
skin surface markers for image registration, in order to eliminate motion
artifacts that could prejudice the analysis. In another work, Gerasimova
et al. [26] considered a larger sample, confirming previous results [25].
Baffa and Lattari [11] used deep learning (Convolutional Neural
Network - CNN) to classify patients into healthy and unhealthy, using
the ITs obtained by DIT (for final diagnosis) and SIT (for initial screening
of cases), from the DMR-IR database [66]. In addition to assessing the
2
Computers in Biology and Medicine 135 (2021) 104553
correctness rate of the classification, the training time of the neural
network was recorded. For the images obtained by DIT, four strategies
were employed to generate a single image that would feed the neural
network. They obtained 98% of average accuracy with DIT images and
95% with SIT images.
Fernández-Ovies et al. [21] also employ CNN for early detection of
breast cancer by thermal images from the DMR-IR database. They
applied the Fast. ai and Pytorch libraries and different architectures of
convolutional neural networks were compared. Their best results were
obtained with resnet34 and resnet50, reaching a predictive precision of
100%.
Tello-Mijares et al. [79] used, as in the two previous studies, the
DMR-IR database to test and evaluate the methodology developed. The
authors compared the performance of four classifiers: CNN, random
forest, multilayer perceptron, and Bayes network. 100% accuracy was
achieved with CNN.
Silva et al. [70] used Support-Vector Machines (SVM) classifier to
classify patients as healthy or with breast abnormalities. Their first step
is the definition of the Region of Interest (ROI) of each sequence of
images. From the ROI, temperature time series were built and several
features were calculated. Before classification by SVM, the main features
were automatically selected. Using the DMR-IR database [66], the au­
thors achieved 100% accuracy.
Considering only the final identification of carcinoma, a very effi­
cient convolutional neural network (CNN) approach with exponential
linear unit and rank-based weighted pooling was presented by Zhang
et al. [86].
Table 1 presents a summary of the related work indicating the year,
the general goal (screening and diagnosis), the image acquisition pro­
tocol (SIT and DIT), number of samples (healthy, benign tumor and
malignant tumor), image acquisition position: frontal (F) and lateral (L),
and the use of the Database for Mastology Research with Infrared Image
(DMR-IR).1
Analyzing this table, we observe that only Baffa and Lattari [11]
explore the combination of SIT and DIT protocols for screening and
diagnosis of breast cancer and only two studies: Silva et al. [70] and
Zhang et al. [86] used balanced databases. Besides that, some related
studies employ complex machine learning techniques to aid in diag­
nosis. We will see in the following sections that our work uses SIT and
DIT protocols for screening and diagnosis of breast cancer, balanced
databases and simpler machine learning techniques than deep learning.
3. Materials
The images used in this work are available at the DMR-IR database.
The DMR-IR images and their use for research have been approved by
the Research Ethical Committee, this is registered under the number
(CAAE: 01042812.0.0000.5243) at the Brazilian Ministry of Health
platform.2 This approval in Brazil is only possible after the acquisition
protocol and the complete project were considered safe. This is a kind of
guarantee that the acquisition of the images does not result in any
damage to the health of the patients participating in the research.
DMR-IR was developed for the management and recovery of breast
exam information and clinical data of volunteer patients. Its purpose is
to support the scientific community in the development and comparison
of computational methodologies that aid the detection and diagnosis of
breast diseases, especially cancer. DMR-IR contains images acquired
following two procedures: Static Image Thermography (SIT) and Dy­
namic Image Thermography (DIT).
Each patient performs the image acquisition using both procedures
1
Database for Mastology Research with Infrared Image (DMR-IR) is available
at http://visual.ic.uff.br/dmi.
2
Brazilian Ministry of Health platform is available at http://plataformabra
sil.saude.gov.br.
R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

Table 1
Comparison of related work using thermographic images (F - frontal; L - lateral). *Zhang et al. use more than one database.
Authors Year Screening Diagnosis DIT SIT Number of Samples Acquisition DMR-IR

Healthy Benign Malign Position Database

Arora et al. [10] 2008 X X X – 34 60 F+L No

Wishart et al. [84] 2010 X X X – 41 65 F+L No
Gerasimova et al. [25] 2014a – X X – 3 – 6 F No
Gerasimova et al. [26] 2014b – X X – 14 – 33 F No
X – – X 177 42

Baffa and Lattari [11] 2018 – X X – 95 – 42 F Yes

Fernández-Ovies et al. [21] 2019 X – – X 175 41 F Yes
Tello-Mijares et al. [79] 2019 X – – X 35 28 F Yes
Silva et al. [70] 2020b X – X – 32 32 F Yes

Zhang et al. [86] 2020 – X Not specified 240 – 240 F Yes*

on the same day. Firstly, each patient is examined by SIT and then by
DIT, following the protocol described in Ref. [66]. It is also important to
mention that both acquisitions are carried out in the same room, under
the same thermal conditions as well as by the same trained team.
Furthermore, it uses the same equipment: a FLIR camera, model SC620
with a resolution of 640 × 480. All acquired images are stored in
DMR-IR that contains 296 patients.
According to the DIT protocol [66], the patient remains standing
with hands on her/his head in an environment with controlled tem­
perature, from 20◦ C to 22◦ C. During this time, the region of the breasts
and armpits of the patients are cooled by an electric fan for a maximum
period of 5 min, or until the patient’s average temperature reaches
30.5 ◦ C. According to the physicians who collaborate in our research
group, such cooling does not present risks to the patient because it is
only superficial. After cooling, 20 images are acquired in sequence
(using 15 s of interval between each acquisition). After testing several
different types of thermal stress, the use of the electric fan was the one
that presented satisfactory uniformity with the least possible discomfort,
greater safety and faster execution of the exam.
The SIT protocol, described in Silva et al. [66], is performed with the
patient acclimatized in a natural manner with hands on the head for 10
min in a room with a controlled temperature between 20◦ C and 22◦ C.
After this step, five images are acquired (one frontal, two laterals of the
left at 45◦ and 90◦ , and two laterals of the right at 45◦ and 90◦ ) with the
patient standing. Only the frontal images are used in this study because
they contain information of anomalies in both breasts. Fig. 1 shows the
exam acquisition. In the image on the camera screen, the temperature of
each point is represented by a color, according to the vertical temper­
ature scale in the right of the thermogram. In this image, the scene points
representing the lowest temperatures are indicated by the dark blue
color, the points of the scene representing intermediate temperatures are
indicated by the light blue, green, yellow and red colors, the points of
the scene representing the higher temperatures are indicated by colors
close to white and white itself.
In this work, 1400 DIT and 80 SIT images were randomly selected
(according to selection criteria) from DMR-IR. For DIT (used for breast
screening), we randomly selected 70 patients (20 images per patient),
where 35 were healthy and 35 had a breast anomaly (benign or malign).
Some these anomalies were: fibroadenomas, nodules, papillary
discharge of serous fluid, phyllodeal tumor of the breast, cysts, ductal
hyperplasia, residual carcinoma, papilliferous carcinoma, infiltrating
ductal carcinoma and lobular carcinoma in situ. For SIT (used for cancer
diagnosis), we randomly selected 80 patients (80 images), where 40 did
not have cancer and 40 had confirmed cancer diagnosis (using biopsy).
4. Proposed methodology
In this work, we propose a hybrid methodology for screening and
breast cancer diagnosis using DIT and SIT protocols, respectively. Fig. 2
depicts these two main phases. In the first phase, seventy (70) patient
DIT data are used to develop the screening methodology. Subsequently,

Fig. 1. Thermography imaging of the breasts of a patient. Fig. 2. General flow of the proposed hybrid methodology.

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R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

eighty (80) patient SIT data are used to develop the diagnostic proposed
in the second phase.
For both steps, the image segmentation process was performed
manually using image editing software. There are cases, like the ones
shown in Fig. 3, that the breasts present alterations, impairing a proper
execution of an automated segmentation of the region of interest (ROI)
[16,50–52,56].

4.1. Screening phase using DIT

Fig. 4 depicts the screening phase in detail. The following subsections

describe the remaining steps of this methodology.

4.1.1. Pre-processing
One of the actions performed in the pre-processing step is the
registration of the 20 DIT images. Image registration is a process of
pairing two or more images of the same scene acquired at different
times, positions, or sensors. One of these images is defined as a reference
and the other as a transformable image. There are several approaches to
image registration. One of the possible registration process seeks an
optimal mapping function T to align the transformable image to the
reference image. This process is named Intensity-based image registra­
tion, it compares and analyzes the corresponding areas in the trans­
formable image to better match the reference one [38,53].
During image acquisition, small movements of the patient’s body
cause differences in the image sequence. We treated these differences
using an image registration algorithm over grayscale DIT images where
the first image is the reference image and the others are transformable.
The image registration uses similarity measures based on the pixel
intensity.
Image registration is done in two stages. In the first stage, the mutual
information (MI) is used as global measure of pixel similarity between
images. The resulting process is the image transformation to be per­
formed in the transformable image. Equation (1) shows the MI between
two images X and Y:
MI(X, Y) = H(X) + H(Y) − H(X, Y) (1) Fig. 4. Screening phase flow.

where H(X) and H(Y) are the entropy of images X and Y, respectively, In the second stage, the local pixel intensity similarity measure
and H (X, Y) is the combined entropy of images X and Y, described in described by Krzanowski and Lai [46] is used as objective function
Equation (2): (Equation (3)).
∑∑
H(X, Y) = p(x, y)log2 (p(x, y)) (2) ∑ N ( t 2)
(qn ⋅r)
x∈X y∈Y E(T) = log ; r = I − J(T) (3)
n=1
α+1
where, p (x, y) is a probability density function [49].
where N is the number of image pixels, qn are eigenvectors in Q (Q is the
set of basis eigenvectors), r is the residual vector (difference image) that
depends on the transformation T and α is a trade-off parameter. The qt
matrix is the transposed matrix of qn. A side-effect of image registration
is to change pixel intensity used to build the time series. Despite this, it
did not change the time series patterns. This measure considers the
complex distortions of intensity varying spatially in the image.

Fig. 3. Patients with alterations in the breasts. Fig. 5. Example of image registration result.

4
R. Resmini et al.
Fig. 5 shows the subtraction of the first and last image in the time
series. Fig. 5a and b shows the results without and with image regis­
tration, respectively. It is possible to notice that Fig. 5b difference is
much smaller that the difference shown in Fig. 5a. However, to measure
the effectiveness of registering images, we use the following measures of
similarities between images: Peak Signal to Noise Ratio (PSNR) [41],
Mean-Square Error (MSE) [60] and Structural Similarity Method (SSIM)
[87]. The more similar two images are, the higher the PSNR value, the
closer to 0 (zero) is the MSE value, and the closer to 1 (one) is the SSIM
value. The results, for the images in Fig. 5, are presented in Table 2. For
all similarity measures, it is possible to see, through the results, the in­
crease in similarity between the images, after registration.
Another action performed in the pre-processing in this phase of the
methodology is ROI segmentation. The segmented ROI is composed of
both breasts. An example of the segmentation result can be seen in
Fig. 6a. The segmentation mask is generated only from the first image in
the sequence of 20 images. Since all images are already registered in
relation to the first, the same mask will be used for all images in the
sequence.
4.1.2. Building the temperature time series
After image registration, the patient’s temperature time series con­
struction comprises the following steps:
1. The region of the breast of the first image sequence is segmented in
order to create a mask, as shown in Fig. 6a. Such mask is applied to
all DIT image sequence.
2. The segmented image region is divided into a grid of 11 × 11 pixels’
squares Rk, with k = 1, 2, …, p, where p is the amount of squares, as
shown in Fig. 6b. Other Rk sizes were tested (such as 3 × 3 and 5 × 5),
but the size of 11 × 11 pixels has shown better results.
3. The higher temperature of each square Rk in all 20 images of the
sequence is used to form the Sk = (tk,1; tk,2; …; tk,20) time series. That
is, tk,1 is the highest temperature in square Rk in the first image of the
sequence, tk,2 is the higher temperature in square Rk in the second
image of the sequence, and so on.
4.1.3. Computing features from DIT
In the initial phases of the research, temperature time series of pa­
tients with and without breast abnormalities were analyzed and the
following hypothesis was obtained:
1. For healthy patients, the temperature time series are more similar
and if clustering algorithms were applied, they would generate
groups that are less compact and closer to each other;
2. For unhealthy patients, there is a group of temperature time series
that stands out from the others and if clustering algorithms were
applied, they would generate more compact and less close groups to
each other.
Based on these observations, the k-means algorithm was applied over
the set of time series, producing k clusters (k ∈ {3, 4, 6, 7, 8, 9, 10}). The
goal is to evaluate the formed groups, with grouping evaluation indexes,
identifying the degree of compactness and distance of such groups. Such
an algorithm has been chosen because it revealed good results in the
tests performed, in the task of grouping time series of similar tempera­
tures. The proximity measure used in the k-means algorithm was the
Table 2
Similarity measures between the images shown in Fig. 5 before and after
registration.
Before registration After registration
PSNR 15.21 21.72
MSE 1956.70 437.86
SSIM 0.79 0.96
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Computers in Biology and Medicine 135 (2021) 104553
Fig. 6. Mask and square grid.
Euclidean distance [24]. Other information about the use of k-means is:
use of all data to build the clustering model; number of seeds equal to ten
(10); number of iterations equal to five hundred (500); random initial­
ization method and; on average ten thousand (10,000) time series of
input for the algorithm. Thus, for a given patient i, the times series built
in the previous step is named Xi = S1; S2; …; Sm, where Sp = (tp,1; tp,2; …;
tp,20), 1 ≤ p ≤ m, is a temperature time series. So, the building process of
the features is performed in the following sequence.
1. The k-means algorithm is performed for k on set Xi and generates
cluster Pi,k. Initially k assumes value 3.
2. The validation index Weighted inter-intra (Strehl) [44] is applied to
measure the quality of the clusters formed in group Pi,k, in order to
measure how compact and well-separated the clusters are. The re­
sults are stored in vector Vi.
3. The value of k is increased by 1 and steps 1 and 2 are performed again
until k = 10.
At the end of all the iterations of the k-means algorithm, vector Vi has
7 features Vi = (vi,1; vi,2; …; vi,7) with vi,j ∈ [0, 1]⊂R, ∀j ∈ [1, 7]⊂N.
4.1.4. Identification of abnormal patients
After the application of unsupervised machine learning techniques to
separate the time series and evaluate the formed clusters, the identifi­
cation of abnormal patients is performed considering the feature vector,
built in the previous stage. For a given patient i vector Vi = (vi,1; vi,2; …;
vi,7) is subjected to the classification model built by K-Star algorithm
[15], which, according to the values contained in Vi, will classify the
patient as healthy or with abnormality (benign or malignant breast
changes), based on the hypothesis described in Section 4.1.3. The K-Star
(or k*) algorithm uses a function based on Kolmogorov distance [45] to
calculate the distance between the instances and perform the
classification.
In order to define the classifier, its parameters, and the features of
vector Vi, for each patient i, Auto-WEKA [80] and Weka [28] were used.
Auto-WEKA was performed on the set of patients. The classifiers and
methods for selecting the features tested are shown in Table 3. The
10-fold-Cross-Validation evaluation method and the execution time of
24 h were used as input parameters for the execution of Auto-WEKA.
Table 4 shows the feature selection method and their parameter
values recommended by Auto-WEKA. The CFS (Correlation based
Feature Selection) algorithm aims to identify a subset of features that are
highly correlated with the class, but that are less correlated with each
other [29]. Vector Vi, for each patient i, is formed by the features
selected from the last line of Table 4. Therefore, we chose the K-Star
classifier and the Strehl index for the breast screening phase.
4.2. Cancer diagnosis phase using SIT
This section presents the methodology developed for diagnosis of
breast cancer, illustrated in Fig. 7. In this phase, the temperature
matrices were used to generate, segment and register the regions of
R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

Table 3
Classifiers and feature selection methods tested in Auto-WEKA [67].
Classifiers

Bayes Net, Naive Bayes, Naive Bayes Multinomial,

Gaussian Process, Linear Regression, Logistic Regression,
Multi-Layer Perceptron, Stochastic Gradient Descent,
Support Vector Machine, Simple Linear Regression,
Simple Logistic Regression, Voted Perceptron,
K-Nearest Neighbors, K-Star, Decision Table,
Repeated Incremental Pruning to
Produce Error Reduction (RIPPER), M5 Rules, 1-R,
Projective Adaptive Resonance Theory (PART), 0-R,
Decision Stump, C4.5 Decision Tree, Logistic Model Tree,
M5 Tree, Random Forest, Random Tree,
Reduced Error Pruning Tree (REP Tree),
Locally Weighted Learning,
AdaBoost M1, Additive Regression,
Attribute Selected, Bagging, Classification via Regression,
LogitBoost, MultiClass Classifier,
Random Committee, Random Subspace,
Voting, Stacking
Feature selection methods
Best First, Greedy Stepwise, Ranker,
Correlation based Feature Selection (CFS) Subset Eval,
Pearson Correlation Eval, Gain Ratio Eval,
Info Gain Eval, 1-R Eval, Principal Components Eval,
RELIEF Eval, Symmetrical Uncertainty Eval.

Table 4
Auto-WEKA recommendations and selected features [67].
Auto-WEKA recommendations

Feature search method Best First

Parameters -D 2 –N 3
Feature evaluation method CFS Subset Eval
Parameters -M -P 0 -E 0
Classifier K-Star
Parameters -B 74 -E -M n
Selected features
Indexes \ k value 2 3 4 5 6 7 8 9 10
Silhouette x
Davies-Bouldin
Calinski-Harabasz
Fig. 7. Cancer Diagnosis flow.
Dunn
Krzanowski-Lai In the diagnosis methodology, we use the log-polar transformation
Hartigan
from the Cartesian coordinates to register the images as described in
Homogeneidade x x
Separação Ref. [64]. Besides, a linear interpolation was performed to complete the
Hubert-Levin x x x transformation process and to map the segmented image’s intensity
Strehl x x x x x x x values into polar coordinates. Fig. 8 shows an example of an image in
which (a) shows the mask generated from segmentation process and (b)
the polar coordinate image used in the registration process.
interest of the images. After this step, several groups of features are
computed. Each group is composed by features based on different ap­
4.2.2. Computing features from SIT
proaches. These groups are then used in the feature selection and clas­
The literature contains several surveys on the use of feature extrac­
sification processes using a Genetic Algorithm (GA) and the Support
tion for the analysis of medical images that expose different types of
Vector Machine (SVM) classifier. The next sections describe these steps
descriptors [14,54,71]. Each one produces a base of features used by the
in detail.
supervised learning algorithms (GA and SVM) to provide the patient’s
diagnosis. This work meets four different approaches to compute
4.2.1. Pre-processing steps
The techniques described in this phase use the temperature values
obtained through SIT. For each image used in this step, the temperature
matrix is collected and used in the ROI segmentation and registration
processes. Note that this phase diverges on ROI definition and regis­
tration approaches. Now, these steps are done considering each breast
side of the same patient. In the screening methodology, they are made
with both breast sides along with a series of images when time goes by.
In this step, for each breast side, the segmentation process results in a
binary image covering the breast region used as a mask. The tempera­
ture points, in the thermal matrix, over this mask are considered as the
ROI. To compare the left and right breast sides, a usual step, after the
segmentation process, is to register the images. Fig. 8. Registration of the right breast used in this step: (a) Breast mask, (b)
Breast in polar coordinates.

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features, which are:

1. Gray Level Co-occurrence Matrix (GLCM) [30];

2. Local Ternary Pattern [78];
3. Daubechies Wavelet [81];
4. Higuchi and Petrosian Fractal Dimensions and Hurst Coefficient [37,
39,57].

The idea of combining these features aims to identify which category

of descriptors is best suited for use with thermal images for the analysis
of breast cancer.
Gray Level Co-occurrence Matrix (GLCM): One of the most used
approaches for computing texture descriptors is the Gray Level Co-
occurrence Matrix, also called Simultaneously Occurrence Matrix. It
consists of quantifying the gray level transitions between pixels that
occur in an image. The calculation considers two parameters: direction
and distance to analyze the behavior between two pixels. These pixels
are called reference and neighbor pixels. In this way, GLCM can compute
the probability of these two pixels occurring simultaneously in an image,
considering the defined direction and distance parameters. The interval
between the reference pixel and the neighboring pixel is given by d in
the expression: P (i, j) d θ. Where P (i, j) is the reference pixel, i and j
define its position in the image (row, column). The elements of the set
d and θ represent, respectively, the distance (in pixels) and the angle of
the reference pixel to the neighboring pixel. Fig. 9 shows the process of
calculating the co-occurrence of gray tones in an image.
By computing the co-occurrence of these two pixels, the size of the
GLCM is directly associated with the number of gray tones present in the
image. Therefore, an image with 256 Gy levels will present a square
matrix with size 256 × 256. After the computation of the GLCM, its
values are usually normalized, and then some features for texture
analysis are computed [30,31].
Second-order statistical features such as Haralick’s texture de­
scriptors have been among the most used descriptors in texture analysis
for a long time [4,18,52]. This type of descriptor interprets the occur­
rence of events in the texture according to the variation of gray tones
and the position in the image.
Local Ternary Pattern (LTP): He et al. [32,33] proposed a tech­
nique in which a mask slides over the image by calculating a ternary
code that represents the pixel and its neighborhood. This code represents
the Texture Unit (TU) and the composition of all texture units is called
the Number of Texture Units (NTU). Subsequently, Ojala et al. [55],
proposed a variation of this technique with a binary code and a certain
degree of relaxation for the calculation. They called it the Local Binary
Pattern (LBP). Tan et al. [77] proposed another variation of the tech­
nique returning to being a ternary code, Local Ternary Pattern (LTP),
using the relaxation of the LBP and variation of the distance from the
neighborhood. LTP is used in this work and is explained as follows.
Fig. 10 shows a 3 × 3 pixel cutout of a sample image. Each value in
the matrix corresponds to a tonal level of a gray scale image.
Fig. 11 shows the mask used to slide through the image starting in
LTP order 0.
Based on the central pixel (g0) the threshold for each neighbor (ei) is
Fig. 10. Image sample in gray scale.
Fig. 11. LTP mask.
calculated.
⎧
⎨ 0, ifgi < g0
ei = 1, ifgi = g0
⎩
2, ifgi > g0
Fig. 12 shows the LTP order used to calculate each neighborhood
value.
The threshold value from the previous step is applied in the LTP for
texture codification. In this example we have 00 × 30 + 02 × 31 + 02 ×
32 + 01 × 33 + 00 × 34 + 00 × 35 + 02 × 36 + 00 × 37 = 1509. The total
size of the spectrum is 6560 possible positions. With each calculation,
the code found is incremented by one in the spectrum.
This procedure describes the calculation of the pixel code for an LTP
spectrum using the order LTP 0. To calculate the other seven possible
spectra, a rotation in the starting position is applied. Fig. 13 shows the
order LTP 4 to illustrate this rotation.
Although most studies that use features based on the number of
texture units are for facial recognition, there are some that use this type
of features with thermal images [58,61]. In general, LTP-based features
are good at determining region boundaries and the trend of their ge­
ometry, such as horizontal or vertical patterns.
Wavelets: Wavelets are sets of mathematical functions used in rep­
resenting data or other functions. They are a method of transforming
signals and time or space-dependent functions. The Wavelet Transform
decomposes the signal according to the spatial frequency. Each
decomposition represents the characteristics in a given frequency range.
In contrast to the traditional Fourier Transform, where the essential

Fig. 9. Example of calculating the GLCM. Fig. 12. LTP order 0.

7
R. Resmini et al.
Fig. 13. LTP order 4.
functions are defined only by the frequency parameter, the Wavelet
Transform considers two parameters: position and scale. This allows the
analysis of local phenomena of a function using fewer degrees of
freedom. It also allows computing features of an examined signal ac­
cording to a particular position and size. In this work, we used a Dau­
bechies wavelets [81].
A striking point in the wavelet approach is that it is able to represent
the image very well according to average coefficients and coefficients of
details. Combined with the multi-resolution technique, Wavelets can
decompose the image into several levels (resolutions). Sathish et al. [61]
and Pramanik et al. [58] used wavelets with thermal images.
Fractal Dimensions: Algorithms for analyzing the fractal dimension
can quantify the degree of irregularity in natural and artificial signal
phenomena. In this study, three fractal measures were used:
1. The Higuchi Fractal Dimension (HFD);
2. The Petrosian Fractal Dimension (PFD);
3. The Hurst coefficient (H).
They are already used in the literature for cancer detection with
thermal images [19,22,42,65,82].
Based on these techniques, seven sets of features were created in this
step. These sets consist of the union of one approach or more. The cre­
ation of these groups allows to evaluate the behavior of the models
under different features and to infer the approach of the extracted fea­
tures that are better suited to the cancer detection process. The features
were extracted separately from each breast of the same volunteer and
were taken to the classifier in the same tuple. The following groups were
formed:
Fractals þ Wavelet + 8 LTP: For this first set of features, the image
was transformed into a 1D spectrum and then applyied decomposition
by Wavelets. In each one, fractal measurements were computed. For the
transformation of the image in the 1D spectrum, LTP was used with
distances x and y varying between 0 and 1, respectively, to cover only
the neighbors closest to the pixel (8 neighbors). The LTP result is a one-
dimensional matrix and was treated as a 1D signal. Eight spectra were
created for each image. For each spectrum, seven wavelet decomposi­
tion levels were applied. Thus, each LTP generated seven signals with
the coefficients of details and one more signal with approximation co­
efficients. At the end of the computation of the described features, 384
features were organized in a tuple (feature vector):
1. LTP: 8 (8 variations of the zero positions (see Fig. 14));
2. Wavelets: (7 coefficients of details + 1 coefficient of approximation);
3. Fractals: 3 (H + HFD + PFD);
4. Breast sides = 2 (left and right).
Fractals + 8 LTP: This set uses same strategy to that of the first set,
except for Wavelets. Thus, 8 LTP were calculated, and then 3 fractal
measures (HFD, PFD, and H) were computed for each LTP and both
breast sides, resulting in 48 features.
GLCM: In this group, four directions (0Âř, 45Âř, 90Âř, and 135Âř)
8
Computers in Biology and Medicine 135 (2021) 104553
Fig. 14. LTP starting at position 0 and LTP starting at position 4.
were considered in the GLCM computation. The d used was 1. After
calculating the GLCM probability matrix, six features were computed,
which according to Ref. [12] are the most relevant Haralick descriptors:
Angular Second Moment, Entropy, Contrast, Variance, Correlation, and
Homogeneity. The total of features of this set was 48 (6 features × 4
angles × 2 breast sides). Fractals + 2 LTP þ GLCM: In this group 2 LTP
order were calculated, named 0 and 4, as shown in Fig. 14. From each of
these LTP orders, the Fractal measures were computed (3 fractals) for
each breast side, generating a total of 12 features. Besides, this group
also combines the features computed from the GLCM. Therefore, a total
of 60 features were computed for this set.
Fractals + 3 LTP: To improve the LTP results without adding too
many features, this set was composed of 3 LTP orders, using the LTPs
labeled 0, 3, and 6. After transforming the images in 3 LTP orders, the
fractal measures were also computed. This strategy resulted in a set with
18 features.
8 LTP: In this group, eight LTP spectra are created. Features pro­
posed specifically for use with LTP are extracted for each spectrum:
Micro Horizontal Structure, Micro Vertical Structure, Micro Diagonal
Structure 1, Micro Diagonal Structure 2, Central Simmetry, Black-White
Symmetry, in addition to 2 features computed from each image: Geo­
metric Simmetry, Degree of Direction [32,55]. This strategy resulted in a
total of 100 features {[(6 features × 8 spectra) + 2 features from the
whole image] × 2 breast sides}.
GLCM + 8 LTP: This set joins the measures computed in the previous
group to those calculated by GLCM, consisting of 148 features.
Several studies have used the SVM classifier in this context
(screening and diagnosis) due to its robustness and suitability to solve
complex problems [1,3,4,27,59]. Based on that, we use each set of
features in the supervised learning process through the execution of the
SVM classifier. For a given set of training cases, SVM builds a model that
assigns new cases to trained classes. The method’s optimal separation is
defined as the best margin positioned between the closest points be­
tween them, called support points.
Model training may require the configuration of several parameters,
and depending on the configuration, it can be quite expensive, but in
general, its performance is high [76]. We use the radial kernel (RBF)
because it is more robust than linear kernel and has lower computational
cost than the polynomial and sigmoidal kernels. In this study, this task
can be outlined, as shown in Fig. 15. The first step is responsible for
configuring the classifier by defining the values for each parameter.
Then, the models for each group of features, summarized in Table 6, are
trained. Part of these features, that are not used in training, is applied in
the newly trained classifier to test its performance. Finally, the model
analysis is carried out according to several performance metrics. At the
end of this cycle, for each new classifier configuration, a new model is
generated. This step outputs ten models that best adapt to the classifi­
cation problem presented (better performance) for each group of fea­
tures, producing seventy better adapted models.
4.2.3. Feature selection and diagnosis
After obtaining the best models for each group of features, the
methodology proposed in this study performs a feature selection
R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

Fig. 15. Model training flow.

Fig. 16. Genetic Algorithm steps.

process. For this, we implement a genetic algorithm (GA). A reason for
selecting features is to decrease the computational cost. Also, with the
screening phase, we use the K-Star classifier under temperature time
reduction in the number of features, the classification process can
series from DIT images, and during the diagnosis phase, we extract
improve the results [48,76]. During the feature computing process,
texture features from SIT images and use the SVM classifier with the RBF
redundant attributes are often calculated, with no influence on learning
kernel.
[85]. The use of GA to perform the feature reduction is well discussed in
We evaluated the results in both phases using the Area Under the
the literature[2,17,73,74]. There are several techniques to perform this
Curve (AUC). The AUC is a measure indicated for both: balanced and
process. One of them is selecting features based on the classification
unbalanced databases. It uses the sensitivity (SEN) and specificity (SPE)
where the classifier itself evaluates the best subset of features.
[47]. SEN is the ability to detect the disease among patients with ab­
The sets of features computed in this study are used as input for the
normalities (Equation (4)) and SPE is the ability to be negative when the
GA that selects the best among them. Only the active features are used in
patient does not have the disease (Equation (5)).
the individual’s evaluation task (classification). The objective function is
a classification task performed with SVM and stratified cross-validation TP
SEN = (4)
with 4-folds. The best combination of the model and set of features is TP + FN
chosen as the ideal solution. The highest mean AUC value measures the
combination. TN
SPE = (5)
In this GA, the initial population is randomly generated, and all ten TN + FP
models are tested. At each interaction, the result is evaluated, and a new
where True Positives (TP) indicates the number of patients correctly
population is formed by the survivors in an elitist strategy, selecting the
classified with the disease, False Positives (FP) is the number of patients
20 best organisms (features) of the generation. Reproduction is per­
wrongly classified as healthy, True Negative (TN) indicates the number
formed by a sexual approach only, by recombination. Forty new or­
of patients wrongly classified with the disease and False Negative (FN) is
ganisms are generated, 20 based on an elitist strategy (20 best crossing
the number of patients wrongly classified as healthy.
each other) and 20 coming from the crossing of the ten best with ten
Moreover, we use accuracy (ACC) to evaluate the correct predictions
worst individuals. Among them, the best individual crosses the 19th, the
in relation to the tests performed (Equation (6)) and precision (PREC) to
2nd with the 18th, etc.
measure the proximity of the correct predictions (Equation (7)).
Each parent contributes to part of the genetic load. The minimum
number of genes for one of the parents is 6, by design decision. The rest ACC =
TP + TN
(6)
of the genetic material comes from the second parent. There is only one TP + FP + FN + TN
crossing point, chosen randomly, which defines the size of each part of
TP
the genetic material of each parent. The GA performs six mutations: PREC = (7)
TP + FP
1. Two mutations in the elite (top ten); In our previous screening studies, we obtained ACC between 86.36%
2. Two mutations among the ten worst; and 91.90%, considering the results of all tested classifiers [69], and,
3. Two mutations among the rest of the population. subsequently, we achieved an average ACC of 95.38% [67]. In the
current work, the screening classification model reached a mean ACC
For each mutation, the genes that will mutate are selected randomly. equal to 98.57%, as shown in Table 5, considering leave-one-out and
As the individual is composed of active and inactive genes, the mutation 10-fold cross validation. This result can be explained by the Strehl index
process reverses the gene’s status. (see Section 4.1.3), which weights intra-group and inter-group similar­
With the steps described up to this point, the new population has 66 ities by the size of each group involved in the calculation of such simi­
individuals. The rest of the population is generated randomly. If the larities. Fig. 17 depicts an example of Strehl index for k = 3, showing its
performance does not improve (repeat the same AUC result for five ability to discriminate healthy patients from patients with breast
consecutive times), a disturbance event is generated in which only the
best individual survives, and all the rest are generated randomly. This
GA iterates through 100 generations of 140 individuals each. Fig. 16 Table 5
Results obtained (in%) for breast screening classification by K-Star method using
illustrates the steps of the genetic algorithm used in this study.
DIT.
Cross-Validation ACC SEN SPE PREC AUC
5. Results and Discussion
Leave-One-Out 98.57 97.14 100.00 98.60 100.00
In this work, we propose a hybrid methodology (1) to screen breast 10-fold 98.57 97.14 100.00 98.60 99.00
Average Result 98.57 97.14 100.00 98.60 99.00
anomalies and (2) to diagnose a cancerous tumor in the breast. In the

9
R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

Fig. 17. Strehl Index to distinguish health patients and patients with breast
abnormalities. Fig. 18. AUC measure with and without feature selection.

abnormality.
In the diagnosis phase, we extracted several texture features (see Table 7
Table 6) from SIT images and applied dimensionality reduction in the Final performance results (in %) for cancer diagnosis.
number of extracted features using a genetic algorithm (GA) to minimize Feature Group ACC SEN SPE PREC AUC
measurement costs and increase the classifier’s performance (see Fractals + Wavelet +8 LTP 91.15 91.15 94.23 91.66 91.02
Fig. 18). Fractals +8 LTP 92.69 92.69 97.43 95.83 92.94
Table 7 presents the final performance of the diagnosis phase using GLCM 94.61 94.61 94.87 91.66 94.87
SVM classifier and feature selection generated by GA. In this table, all Fractals +2 LTP + GLCM 88.84 88.84 91.02 87.50 89.10
Fractals +3 LTP 86.66 86.66 97.43 95.83 87.82
groups of features with better AUC values present ACC, SEN, SPE, and
8 LTP 80.64 80.64 82.05 83.33 82.05
PREC greater than 90%, except PREC of feature group GLCM +8 LTP. GLCM +8 LTP 91.66 91.66 92.30 87.50 92.30
For each group of features, the GA selects the features that generate the
best performance (see Appendix A).
The first group of features analyzed in Table 7 refers to the texture In Fractals +2 LTP + GLCM group, features were computed orders
group formed by Fractals, Wavelet, and LTP. In this group, the best 0 and 4 from LTP but were not calculated the Energy and Homogeneity
result obtained was the SPE equal to 94.23% generated by Wavelets descriptors and the direction of 135◦ according to Table 12. The next
composed of the ROI average (or approximation) coefficients plus the two texture groups (Fractals + 3 LTP and 8 LTP) computed fractal fea­
detail coefficients of the Wavelets decomposition of all levels, except at tures from 3 (orders 0, 3 and 6) and 8 (orders 0 to 7) LTP (see Tables 13
level 5 and only the orders 1 and 0 among the 8 LTP features according and 14). These groups generate the worst performance for ACC, SEN,
to Table 9. and AUC measures among the evaluated groups.
The second texture group of Table 7 uses Fractals and LTP features. The last group analyzed in Table 7 (GLCM + 8 LTP) computed eight
In this group, only 3 LTP features were selected (orders 0, 1, and 2) spectra (orders 0 to 7) from LTP and added Angular Second Moment,
according to Table 10, but this feature selection generated the highest Energy, and Dissimilarity in directions 135◦ , 0◦ , and 90◦ described in
SPE and PREC values between groups analyzed. Table 15, respectively. The performance measures of this group showed
The next line of Table 7 presents the results of the GLCM group, values around 91%, except in PREC that obtained a value equal to
through the analysis of Contrast, Dissimilarity, Homogeneity, Angular 87.50%.
Second Moment, Energy, and Correlation descriptors defined by Har­ In the diagnosis phase, the SVM classifier reached an ACC of 94.61%
alick [30,31] under 3 directions (0◦ , 90◦ , and 135◦ ) (see Table 11). This and AUC equal to 94.87% using the GLCM group. The GLCM group
group obtained values above 94% for all measures evaluated, except for presented the best results of ACC, SEN and AUC compared to the other
PREC with a value equal to 91.66%. groups analyzed in the diagnosis phase. Taken together, the results of
the hybrid methodology exploring temperature time series and texture
features pointed to a low cost to identify abnormalities and diagnose
Table 6 cancer from infrared thermal images.
Combinations of texture features.
Feature Group Number of Features 5.1. Comparison with related work
extracted
In Section 2, we presented several studies focused on the abnor­
Fractals + Wavelet +8 LTP 384
malities screening and breast cancer diagnosis and concluded that most
Fractals +8 LTP 48
GLCM 48 of them use unbalanced datasets, do not explore the combination of SIT
Fractals +2 LTP + GLCM 60 and DIT protocols, and do not apply screening and diagnosis method­
Fractals +3 LTP 18 ologies together. Moreover, some studies employ complex machine
8 LTP 100 learning techniques like deep learning. We compare our results to these
GLCM +8 LTP 148
studies and summarize these comparisons in Table 8.

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R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

Table 8 temperature during a cooling or homeostasis process, allowing the

Comparison with related work. detection of tumors through analysis of thermal images.
DMR-IR We used SIT and DIT protocols to acquire these images. We processed
DIT images using temperature time series to identify abnormalities in
Author DIT SIT SEN (%) SPE (%) ACC (%) Database
patients’ breasts during the first phase of this study. In the second phase,
Arora et al. X 97 27 not No we analyzed SIT images by texture features selection using a genetic
[10] informed
Wishart et al. X 70 48 not No
algorithm.
[84] informed In the screening phase of patients with breast abnormalities, the
Gerasimova X 76 86 not No features were values of the cluster validity index. We generated these
et al. [25] informed features through the clustering of temperature time series using the k-
X 97 100 98
means algorithm. We used them in a k-star classifier, and we obtained an
accuracy of 99% in abnormalities (benign and malignant tumors)
Baffa and X 93 98 95 Yes
Lattari [11] detection.
Fernández- X not not 100 Yes The SVM classifier developed in sequence reached 95% accuracy in
Ovies et al. informed informed cancer detection. It performs texture analysis with resources extracted
[21]
by second-order, fractal, and wavelet statistical approaches and explores
Tello-Mijares X 100 100 100 Yes
et al. [79]
genetic algorithms to define relevant features to detect malignant tu­
Silva et al. X 100 100 100 Yes mors. GLCM presented the best performance among the analyzed
[70] texture features.
Zhang et al. Not 94 94 94 Yes The proposed hybrid methodology presented a solid contribution in
[86] specified
abnormalities screening and malignant tumor diagnosis. This work,
X 97 100 99
however, is subject to limitations such as (1) the limited number of
Our work X 95 95 95 Yes patients used, (2) manual segmentation of the regions of interest, (3) use
of a simple distance for the LTP, (4) the number of iterations of the
genetic algorithm, (5) gap of consideration of the linear, polynomial or
Among the related work, we observe that Arora et al. [10], Baffa and sigmoidal kernel in SVM classifier and (6) lack of inclusion or indication
Lattari [11], Tello-Mijares et al. [79], Silva et al. [70], and Zhang et al. of the breast and position of the abnormality.
[86] present SEN greater than 90%, but only Baffa and Lattari [11] uses As future work, we intend to evaluate a classification model that
both SIT and DIT protocols. Besides that, Arora et al. [10], Baffa and considers the differences between left and right breasts, indicating in
Lattari [11], and Zhang et al. [86] perform the diagnostic method, and which breast the abnormality was detected. We have the intention of
only Zhang et al. [86] uses a balanced dataset and does not screen ab­ enlarging the distance among pixels in the LTP approach, increasing the
normalities in patients. In this work, we achieved a SEN equal to 97% in number of iterations of the genetic algorithm in the model selection and
the screening phase and 95% in the diagnosis phase using a balanced using the linear, polynomial and sigmoidal kernels in SVM with a par­
dataset and both protocols filling the gaps of the previous researches. allel implementation to reduce the execution time of the genetic algo­
Regarding the SPE and ACC measures, Baffa and Lattari [11], rithm. It will be useful to indicate the image coordinates (x, y) of the
Tello-Mijares et al. [79], Silva et al. [70] and Zhang et al. [86] reach suspected abnormality, considering DIT and SIT images. The breast re­
values greater than 90%. Among them, only Silva et al. [70] does not use gion segmentation could be improved, by developing a semi-automatic
deep learning. Our results achieved SPE and ACC values above 95% in segmentation method. For patients undergoing neoadjuvant cancer
the screening and diagnosis phases, indicating that our approach is treatment, it would be interesting to have a tumor volume evaluator [9].
promising even compared to methodologies based on deep learning. Finally, we continue acquiring thermal images to increase our DMR-IR
Note that Arora et al. [10], Wishard et al. [84] and Gerasimova et al. database size.
[25, 26] present worst SPE measures. Furthermore, comparing our work
with Baffa and Lattari [11] it is possible to state that the order of DIT or
SIT in the screening and diagnosis phases does not present a difference in Declaration of competing interest
terms of performance.
Our work performs screening and diagnosis, while Zhang et al. [86] This work was not funded by any private or public institution. The
only makes diagnosis and Tello-Mijares et al. [79] only perform financial support was provided from CAPES, CNPq and FAPERJ gov­
screening. Analyzing Fernándes-Ovies et al. [21], we realized that this ernment agencies and CAPES PRINT Project. This research has also been
article presents ACC equal to 100%, but it uses an unbalanced dataset partially supported by project Pro-Engenharia 021–2008 and INCT-
and the ACC is not a good measure of performance in this case [13]. MACC. That is, we wish to confirm that there are no known conflicts
The results obtained in the abnormality screening and cancer diag­ of interest associated with this publication and there has been no sig­
nosis phases demonstrate that the hybrid approach proposed in this nificant financial support for this work that could have influenced its
work presents a significant contribution to research on early diagnosis of outcome.
breast cancer.
Acknowledgment
6. Conclusion
The authors are thankful to the patients who consent on the use of
The human body emits infrared radiation with an intensity propor­ their data for research. R.R., L.F.S. and A.S.A. gratefully acknowledge
tional to its temperature. Cameras sensitive to the infrared spectrum the support from CAPES in their graduation courses. A.C. and D.C.M.S.
capture this radiation and convert it to visual information (thermal thank to CAPES PRINT 88881.310304/2018-01, FAPERJ E-26/
images). Abnormal regions of the breast maintain more constant 010.002431/2019, INCT-MACC, and CNPq 307329/2016-0.

11
R. Resmini et al. Computers in Biology and Medicine 135 (2021) 104553

A Appendix.

The selection of features related to GLCM was commented in Section “Results and Discussion”. Those selected from other groups and even
combination of GLCM plus such groups are presented in Tables 9–15

Table 9
Feature selection for Fractal Dimension + Wavelet +8 LTP Feature.

Feature Wavelet Wavelet Order Breast Side

Coefficient Level

Hurst DET 0 0 Left

Higuchi DET 0 0 Left
Hurst DET 1 0 Left
Higuchi DET 1 0 Left
Higuchi DET 2 0 Left
Petrosian DET 3 0 Left
Petrosian DET 4 0 Left
Hurst DET 6 0 Left
Higuchi DET 6 0 Left
Petrosian DET 6 0 Left
Hurst APP – 1 Left
Higuchi APP – 1 Left
Hurst DET 0 1 Left
Petrosian DET 0 1 Left
Hurst DET 1 1 Left
Petrosian DET 1 1 Left
Hurst DET 4 1 Left
Petrosian DET 6 1 Left

Table 10
Feature selection for Fractal Dimension Feature +8 LTP.

Feature Order Breast Side

Hurst 0 Left
Higuch 0 Left
Hurst 0 Left
Higuch 0 Left
Hurst 0 Left
Higuch 0 Left
Hurst 1 Left
Higuch 1 Left
Higuch 1 Left
Petrosian 1 Left
Hurst 1 Left
Petrosian 1 Left
Higuch 2 Left
Hurst 2 Left
Higuch 2 Left
Higuch 2 Left

Table 11
Feature selection for GLCM.

Feature Angle (◦ ) Breast Side

Contrast 0 Left
Homogeneity 0 Left
Correlation 0 Left
Angular Second Moment 0 Left
Contrast 0 Right
Energy 0 Right
Correlation 0 Right
Angular Second Moment 0 Right
Angular Second Moment 90 Left
Contrast 90 Right
Dissimilarity 90 Right
Energy 90 Right
Angular Second Moment 90 Right
Dissimilarity 135 Left
Homogeneity 135 Left
Angular Second Moment 135 Left
Correlation 135 Right

12
R. Resmini et al.
Table 12
Feature selection for Fractal Dimension Feature + 2 LTP + GLCM.
Feature
Hurst
Higuchi
Petrosian
Hurst
Petrosian
Angular Second Moment
Angular Second Moment
Correlation
Contrast
Dissimilarity
Table 13
Feature selection for Fractal Dimension Features +3 LTP.
Feature
Petrosian
Hurst
Higuchi
Petrosian
Hurst
Higuchi
Petrosian
Higuchi
Table 14
Feature selection for 8 LTP.
Feature
Black White Simmetry
Micro-Vertical Structure
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Micro-Vertical Structure
Micro-Diagonal Structure 2
Central Simmetry
Black White Simmetry
Micro-Vertical Structure
Black White Simmetry
Micro-Horizontal Structure
Micro-Diagonal Structure 2
Central Simmetry
Black White Simmetry
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Micro-Diagonal Structure 2
Central Simmetry
Central Simmetry
Black White Simmetry
Geometric Simmetry
Degree of Direction
Micro-Vertical Structure
Micro-Diagonal Structure 1
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Central Simmetry
Geometric Simmetry
Computers in Biology and Medicine 135 (2021) 104553
Order/Angle Breast Side
0 Left
0 Left
0 Left
4 Left
0 Right
0◦ Left
90◦ Left
45◦ Right
90◦ Right
90◦ Right
Order Breast Side
0 Right
3 Left
3 Left
3 Left
3 Right
3 Right
3 Right
6 Right
Order Breast Side
0 Left
1 Left
2 Left
2 Left
2 Left
3 Left
3 Left
3 Left
3 Left
4 Left
4 Left
5 Left
5 Left
5 Left
5 Left
6 Left
6 Left
6 Left
6 Left
6 Left
7 Left
7 Left
7 Left
7 Left
5 Right
6 Right
7 Right
7 Right
7 Right
7 Right
7 Right
13
R. Resmini et al.
Table 15
Feature selection for GLCM +8 LTP.
Feature
Micro-Vertical Structure
Micro-Diagonal Structure 1
Central Simmetry
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Central Simmetry
Black White Simmetry
Micro-Horizontal Structure
Micro-Diagonal Structure 1
Micro-Diagonal Structure 2
Black White Simmetry
Micro-Vertical Structure
Black White Simmetry
Micro-Diagonal Structure 1
Micro-Diagonal Structure 2
Central Simmetry
Black White Simmetry
Micro-Diagonal Structure 1
Black White Simmetry
Degree of Direction
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Micro-Diagonal Structure 2
Micro-Diagonal Structure 1
Central Simmetry
Micro-Vertical Structure
Micro-Diagonal Structure 1
Central Simmetry
Micro-Vertical Structure
Micro-Diagonal Structure 1
Micro-Diagonal Structure 2
Central Simmetry
Black White Simmetry
Micro-Horizontal Structure
Micro-Vertical Structure
Micro-Diagonal Structure 1
Central Simmetry
Angular Second Moment
Energy
Dissimilarity
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