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Abstract
The aim of the study was (1) to perform an automated segmentation of hot spot regions of the hand from thermograph
using the k-means algorithm and (2) to test the potential of features extracted from the hand thermograph and its measured skin temperature indices in the evaluation of rheumatoid arthritis. Thermal image analysis based on skin temperature measurement, heat distribution index and thermographic index was analyzed in rheumatoid arthritis patients and
controls. The k-means algorithm was used for image segmentation, and features were extracted from the segmented
output image using the gray-level co-occurrence matrix method. In metacarpo-phalangeal, proximal inter-phalangeal and
distal inter-phalangeal regions, the calculated percentage difference in the mean values of skin temperatures was found
to be higher in rheumatoid arthritis patients (5.3%, 4.9% and 4.8% in MCP3, PIP3 and DIP3 joints, respectively) as compared to the normal group. k-Means algorithm applied in the thermal imaging provided better segmentation results in
evaluating the disease. In the total population studied, the measured mean average skin temperature of the MCP3 joint
was highly correlated with most of the extracted features of the hand. In the total population studied, the statistical feature extracted parameters correlated significantly with skin surface temperature measurements and measured temperature indices. Hence, the developed computer-aided diagnostic tool using MATLAB could be used as a reliable method in
diagnosing and analyzing the arthritis in hand thermal images.
Keywords
Heat distribution index, thermographic index, rheumatoid arthritis, k-means algorithm
Introduction
Rheumatoid arthritis (RA) is a chronic autoimmune
disease that causes inflammation of blood vessels,
development of bumps called rheumatoid nodules,
weakening of bones and deformity of the joints leading
to long-term disability. It causes premature mortality,
disability and compromised quality of life in the industrialized and developing world.1 The prevalence of RA
ranges from 0.5% to 1% worldwide in the general population.1 The prevalence rate in India is 0.9%, almost
equal to the world prevalence rate.2 RA is associated
with severe disability and substantial morbidity.3,4
Symmons and Gabriel5 reported that mortality is
greater in patients with established RA in comparison
with the general population. RA directly affects physical function and mobility and results in substantial
short-term and long-term morbidity.
Thermal imaging is a non-contact, noninvasive,
diagnostic imaging procedure based on skin
Corresponding author:
M Anburajan, Department of Biomedical Engineering, SRM University,
Kattankulathur 603203, Chennai, Tamil Nadu, India.
Email: hod.biomedi@ktr.srmuniv.ac.in
320
Snekhalatha et al.
321
5.
6.
Temperature indices
7.
3.
4.
Mean
The mean is the average intensity value of the hot
spot regions and was given as
X X
Mean =
i
jiP(i, j)
2
2.
SD
The SD is a measure of dispersion or variation
from the mean value. A low SD represents the
data points to be very close to the mean value
and a high SD represents the data points are
spread out over the large range of values
s=
N1 N
1
X
X
!1=2
2
(i m) p(i, j)
i=0 j=0
3.
Entropy
Entropy is the measure of randomness that can
be used to characterize the texture of the image.
It is a quantitative measure of image information.
If all the image pixels have the same gray level,
minimum entropy is achieved; if the pixels have a
uniform distribution of gray levels or the image is
histogram equalized, maximum entropy is
achieved
X X
Entropy =
i
jP(i, j) logP(i, j)
4
4.
Skewness
Skewness is the measure of the asymmetry of the
pixel distribution around its mean. A symmetric
distribution has zero skewness and has equal values for mean, median and mode. If the skewness
is positive, then the data are positive skewed or
skewed right, meaning that the right tail of the
322
5.
Kurtosis
Kurtosis refers to the measure of the peak of the
array of intensity distribution. Similar to skewness, kurtosis is a descriptor of the shape of the
probability distribution. There are three different
interpretations of kurtosis: mesokurtic distribution, leptokurtic distribution and platykurtic distribution. A zero excess kurtosis indicates the
mesokurtic distribution which has a normal
peak around the mean. A positive excess kurtosis
represents the leptokurtic distribution which has a
more acute peak around the mean. A negative
excess kurtosis shows the platykurtic distribution
which has a lower, wider peak around the mean29
i
i
Xhh
Kurtosis =
P(i, j) m4 =N =s4 3
6
6.
7.
Variance
The variance is the square of the SD. A small
variance indicates that the data points are close
to the mean, whereas the large variance
means that the data points are spread out from
the mean
X X
Var =
i
j(i m)2 P(i, j)
7
Contrast
The contrast is the measure of the intensity contrast between the pixel and its neighbors
XX
Contrast =
i, j2 Pi, j
8
i=0 i=0
8.
Energy
Energy is given by the sum of the squared elements in the GLCM. Energy measures the textural uniformity that means pixel pairs
repetitions. It also measures the smoothness of
the image. For more uniformly distributed pixels
in image regions, the smoothness level and energy
were low. But in case of the nonuniform distributed region, the smoothness and energy are high.
Hence, in case of RA patients, due to uneven distribution of temperature in hand regions, the
energy obtained was higher compared to the
normal30
Energy =
(Pi, j )2
i, j = 0
9.
Correlation
Correlation is a measure of linear dependencies of
gray level on those of neighboring pixels
Correlation =
X X (i m)(j m)P(i, j)
si sj
i=0 j=0
10.
10
Homogeneity
Homogeneity is used to determine whether frequency counts are distributed identically across
different populations
Homogenity =
N1
X
pij
i, j = 0 1 + i
j2
11
Statistical analysis
Data were analyzed using SPSS software package version 19.0 (SPSS Inc., Chicago, IL, USA). The measured
mean surface temperature, HDI, TI and feature extraction parameters were compared between the RA group
and normal group using a Students t-test. The
KolmogorovSmirnov and ShapiroWilk tests were
performed to test the normality of above-mentioned
variables which gave a significance value (p \ 0.05).
The bi-variate (Pearson correlation) analyses were used
to obtain the correlations between HDI, TI, skin temperature measurements and feature extraction parameters in the total population studied.
Results
HDI and TI analysis
The measured temperature indices correlated significantly with the feature extracted parameters in the total
population studied (Table 1). The mean values of measured HDI and TI in RA patients were highly significant (p \ 0.01) when compared to the normal group.
The mean (6SD) HDI values of both RA and normal
groups were obtained as 0.79 (60.2) and 0.38 (60.1),
respectively, and found to be statistically significant.
Also, the measured mean (6SD) values of TI obtained
for the RA group and normal groups were 4.18 (60.5)
and 2.69 (60.5), respectively (Table 2). The percentage
of patients whose diagnostic values of TI categorized
into normal, osteoarthritis and RA was 24.4%, 8.8%
and 66.6%, respectively.
Snekhalatha et al.
323
Table 1. Correlation matrix between temperature parameter and statistical feature extracted parameter measured from hand
thermal image in total population studied.
Temperature
parameters
Standard
deviation
Skewness
Entropy
Thermal indices
HDI
0.4**
0.42**
0.39*
0.45**
TI
0.46** 0.51**
0.44**
0.47**
Skin temperature at MCP joints, PIP joints and DIP joints
0.32*
0.31*
MCP1
0.45** 0.24#
0.34*
0.21#
MCP2
0.46** 0.25#
MCP3
0.48** 0.51**
0.52**
0.51**
MCP4
0.46** 0.48**
0.48**
0.49**
MCP5
0.41** 0.26
0.42**
0.39*
PIP2
0.3*
0.29*
0.37*
0.27#
0.38*
0.41**
0.26#
PIP3
0.27#
0.26#
0.38*
0.26#
PIP4
0.27#
PIP5
0.3*
0.3*
0.37*
0.31*
0.09#
0.11#
0.2#
DIP1
0.27#
DIP2
0.24#
0.2#
0.24#
0.25\#
#
#
#
DIP3
0.23
0.23
0.27
0.26#
DIP4
0.23#
0.16#
0.31*
0.25#
#
#
#
DIP5
0.22
0.15
0.26
0.26#
Kurtosis
Variance
Contrast
Correlation
Energy
Homogeneity
0.39*
0.44**
0.38*
0.33*
0.56**
0.61**
0.44**
0.53**
0.44**
0.54**
0.45**
0.54**
0.25#
0.20#
0.43**
0.42**
0.26#
0.48**
0.46**
0.48**
0.47**
0.05#
0.22#
0.21#
0.17#
0.14#
0.42**
0.40**
0.31*
0.26
0.39*
0.24#
0.32*
0.24#
0.29*
0.019#
0.05#
0.06#
0.0002#
0.22#
0.25#
0.27#
0.55**
0.53**
0.50**
0.29*
0.38*
0.26
0.25#
0.005#
0.16#
0.15#
0.07#
0.03#
0.30*
0.26#
0.56**
0.30*
0.33*
0.52**
0.56**
0.51**
0.45**
0.03#
0.21#
0.23#
0.24#
0.22#
0.33*
0.28*
0.56**
0.30*
0.28*
0.3*
0.32*
0.29*
0.28*
0.016#
0.12#
0.14#
0.16#
0.12#
0.39*
0.39*
0.56**
0.41**
0.46**
0.32*
0.34*
0.31*
0.29*
0.05#
0.16#
0.18#
0.19#
0.16#
HDI: heat distribution index; TI: thermographic index; MCP: metacarpo-phalangeal; PIP: proximal inter-phalangeal; DIP: distal inter-phalangeal; NS:
not significant.
*p \ 0.05; **p \ 0.01; #NS.
Table 2. Measured mean average skin surface temperature of RA and normal in required region of interest.
Temperature
parameters
Region of
interest
RA (N = 30),
mean 6 SD
Normal (N = 15),
mean 6 SD
% Difference
Statistical
significance (p)
0.38 6 0.1
2.69 6 0.5
51.89
35.64
0.001
0.001
33.93 6 0.3
33.86 6 0.2
33.64 6 0.2
33.76 6 0.2
33.86 6 0.2
33.80 6 0.2
33.71 6 0.2
33.72 6 0.2
33.67 6 0.1
33.87 6 0.4
33.86 6 0.2
33.55 6 0.4
33.57 6 0.3
33.75 6 0.1
34.43 6 0.2
3.84
4.35
5.29
4.44
4.35
4.79
4.88
4.71
4.60
3.80
4.35
4.79
4.68
3.98
2.71
0.002
0.003
0.001
0.003
0.004
0.002
0.001
0.004
0.001
0.005
0.001
0.001
0.004
0.005
0.004
2.89E 2 06 6 1.08E 2 06
2.08E 2 05 6 9.58E 2 06
0.001 6 0.0008
0.0001 6 5.61E 2 05
0.008 6 0.007
4.06E 2 13 6 8.47E 2 13
3.94E 2 08 6 1.37E 2 08
6.94E 2 06 6 2.18E 2 06
0.0004 6 0.0003
0.00044 6 0.0003
0.00046 6 0.0003
94.25
74.59
8.33
95
93.75
50.25
50.27
89.39
75
71.42
76.47
0.0003
0.0002
0.0009
0.0002
0.0004
0.06
0.03
3.66E 2 06
0.0002
0.0004
0.0002
Thermal indices
HDI
Whole hand
0.79 6 0.2
TI
Whole hand
4.18 6 0.5
Skin temperature measurements at joints
MCP
MCP1
35.39 6 0.6
MCP2
35.40 6 0.6
MCP3
35.52 6 0.7
MCP4
35.33 6 0.6
MCP5
35.40 6 0.6
PIP
PIP2
35.42 6 0.6
PIP3
35.44 6 0.4
PIP4
35.39 6 0.4
PIP5
35.22 6 0.7
DIP
DIP1
35.21 6 0.5
DIP2
35.40 6 0.6
DIP3
35.24 6 0.6
DIP4
35.22 6 0.5
DIP5
35.15 6 0.5
Ventral side
palm
35.39 6 0.7
Measured statistical features
Mean
Whole hand
5.03E 2 05 6 5.868E 2 05
Std dev
Whole hand
8.54E 2 05 6 7.63E 2 05
Skewness
Whole hand
0.006 6 0.006
Entropy
Whole hand
0.002 6 0.002
Kurtosis
Whole hand
0.128 6 0.15
Smoothness
Whole hand
5.1941E 2 11 6 1.368E 2 10
Variance
Whole hand
7.924E 2 08 6 9.08E 2 08
Contrast
Whole hand
6.5461E 2 05 6 5.054E 2 05
Correlation
Whole hand
0.0016 6 0.0014
Energy
Whole hand
0.0014 6 0.001
Homogeneity
Whole hand
0.0017 6 0.001
RA: rheumatoid arthritis; SD: standard deviation; HDI: heat distribution index; TI: thermographic index; MCP: metacarpo-phalangeal; PIP: proximal
inter-phalangeal; DIP: distal inter-phalangeal.
Downloaded from pih.sagepub.com by guest on May 1, 2015
324
In MCP, PIP and DIP regions, the calculated percentage difference in the mean values of skin temperatures
was found to be higher in MCP3, PIP3 and DIP3
regions of interests in the RA group, as compared to
the normal group. These values were 5.3%
[((35.52 2 33.64)/35.52) 3 100], 4.9% [((35.44 2 33.71)/
35.44) 3 100] and 4.8% [((35.24 2 33.55)/35.24) 3 100],
respectively, and these values were statistically significant at p \ 0.001. Thus, in the RA group, the MCP3
joint region showed highest percentage difference in the
mean values of skin temperature, as compared to normal group. Figure 1(a) and (b) represents the dorsal
view of the hand thermal image of normal subject and
the RA patient, respectively. In total, 14 ROIs (square
boxes) are shown with the minimum and maximum
skin surface temperatures. These ROIs correspond to
MCP (15), PIP (25) and DIP (15) joints of each
hand of a subject in the RA and normal groups.
Similarly, Figure 1(c) and (d) represents the ventral
Figure 1. (a) Normal subjectdorsal view of the hand thermal image. The square ROIs indicate the boxes depicting the minimum
temperature ranges (30.6 C32.5 C) and maximum skin surface temperature ranges (31.5 C32.5 C) at the MCP, PIP and DIP
joints. (b) RA patientsdorsal view of the hand thermal image. The square ROIs indicate the boxes depicting the minimum
temperature ranges (31.9 C33.6 C) and maximum skin surface temperature ranges (33 C34.8 C) at the MCP, PIP and DIP
joints. (c) Normal subjectventral view of the measured thermal image. The square ROI indicates a box depicting the minimum
temperature (34.5 C) and maximum skin surface temperature (35.9 C) at palm region. (d) RA patientventral view of the hand
thermal image. The square ROI indicates a box depicting the minimum temperature (35.5 C) and maximum skin surface
temperature (36.5 C) at palm region.
Snekhalatha et al.
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Figure 2. RA patientdorsal view of various stages of the segmented output hand thermal image: (a) input hand thermal image, (b)
cluster 1 image depicts presence of hot spot region, (c) cluster 2 image depicts the background, (d) cluster 3 image depicts the other
regions, (e) segmented output image depicts presence of hot spot region and (f) segmented gray output image with hot spot region.
326
Figure 3. Normal subjectdorsal view of the various stages of segmented output hand thermal image: (a) input hand thermal
image, (b) cluster 1 image depicts absence of hot spot region, (c) cluster 2 image represents the background, (d) the cluster 3 image
depicts the other region, (e) segmented output image depicts the absence of hot spot region and (f) segmented gray output image
without any hot spot region.
Snekhalatha et al.
327
Figure 4. RA patientventral view of various stages of the segmented output hand thermal image: (a) input hand thermal image, (b)
cluster 1 image depicts presence of hot spot region, (c) cluster 2 image depicts the background, (d) cluster 3 image depicts the other
regions, (e) segmented output image depicts presence of hot spot region and (f) segmented gray output image with hot spot region.
Discussion
In this study, the mean average skin surface temperature was measured at DIP, PIP and MCP of digits 15
328
Figure 5. Normal subjectventral view of the various stages of segmented output hand thermal image: (a) input hand thermal
image, (b) cluster 1 image depicts absence of hot spot region, (c) cluster 2 image represents the background, (d) cluster 3 image
depicts the other region, (e) segmented output image depicts the absence of hot spot region and (f) segmented gray output image
without any hot spot region.
Snekhalatha et al.
329
Figure 6. A computer-aided diagnostic tool for thermal image analysis of hand-segmented image: (a) sample RA patient and (b)
sample normal subject.
35.5 C. In our study, RA patients had the mean average surface temperature in the ventral side of the hand
as 35.39 C compared with that of the healthy controls
as 34.43 C. The percentage temperature difference
obtained between RA and normal groups was higher
(2.71%) in our study compared to the study conducted
by Borojevic et al. (1.63%). Hence, the reason for
increased temperature in the hands of RA was due to
the increased vascularity caused by synovitis and the
proliferation of synovial cells. Also, the blood flow was
prevented from deep circulation to subcutaneous
330
Conclusion
In conclusion, in the population studied, the measured
mean average skin temperature of MCP3 joint highly
correlated with most of the extracted features of the
hand. Thermal imaging parameters such as skin temperature measurements, TI and HDI correlated significantly with feature extracted parameters in the
population studied. Hence, the developed computeraided diagnostic tool using MATLAB could be used as
a reliable method in diagnosing and analyzing the
arthritis in hand thermal images.
Declaration of conflicting interests
The authors declare that there is no conflict of interest.
Disclosure
This article has been read and approved by all the
authors. This article is not under consideration by any
other publications and has not been published
elsewhere.
Funding
This research received no specific grant from any funding agency in the public, commercial or not-for-profit
sectors.
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