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Infrared Physics and Technology 95 (2018) 203–212

Contents lists available at ScienceDirect

Infrared Physics & Technology


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

Regular article

Establishing the thermal patterns of healthy people from Medellín, T


Colombia☆
María Camila Henao-Higuitaa,b, Alexandra Benítez-Mesaa,b, Hermes Fandiño-Torob,
Adriana Guerrero-Peñac, Gloria Díaz-Londoñoa,

a
Grupo de Investigación e Innovación Biomédica, Instituto Tecnológico Metropolitano, Calle 73 No. 76A-354, Vía al Volador, Medellín, Colombia
b
Grupo de Automática, Electrónica y Ciencias Computacionales, Instituto Tecnológico Metropolitano, Carrera 31 No. 54-22, Medellín, Colombia
c
Grupo de Investigación Didactica y Modelamiento en Ciencias DaVinci, Instituto Tecnológico Metropolitano, Carrera 31 No. 54-22, Medellín, Colombia

ARTICLE INFO ABSTRACT

Keywords: Infrared Thermography has been used in the medical field to diagnose illnesses that produce temperature variations.
Infrared thermography Furthermore, comparisons between the temperatures of contralateral regions or patients and healthy people are used as
Thermal patterns thermography diagnostic criteria. Under both approaches, the difference in temperature is calculated and, if it falls outside
Healthy people normal ranges, it is considered a sign and symptom of illness. In previous works, the thermal patterns of healthy in-
dividuals have been determined in populations from Finland, Portugal, Taiwan, Brazil, and Mexico. However, a com-
parison of such patterns reveals meaningful discrepancies since the emissivity of the human skin depends on ethnic
characteristics and age. Thus, it is necessary to estimate thermal patterns in healthy people from each population and
calculate the maximum and minimum temperature differences in their contralateral regions. Specifically, the thermal
patterns of healthy Colombian people have not been established so far. Therefore, this work aims to define the thermal
patterns of the population of Medellín-Colombia. Such patterns can later be used as reference values to diagnose illnesses
in different hospitals in the city. Thirty-seven healthy individuals participated in this study. Data was acquired from the
anterior, posterior, right, and left side of the body using a FLIR A655SC thermal camera, and the acquisition protocol was
defined in accordance with the method of previous work. The camera recorded twenty-four thermograms from each
subject, which were segmented by region-growing and a grid mask algorithm, thus obtaining 43 regions of interest (ROI).
The mean temperature and standard deviations of each ROI were also calculated. In most regions, the mean temperature
varied between 31.16 °C and 34.58 °C. The lowest mean temperature and highest variability were found in acral regions.
Independent samples were assumed in the statistical analysis, and the normality of the temperature of each ROI was
verified by the Shapiro–Wilk test. Moreover, Student’s t-test and Mann–Whitney U test were used in the comparison of
temperatures of contralateral regions with normal and non normal distributions, respectively. Finally, the temperature
difference was found to be insignificant.

1. Introduction with acute rheumatoid arthritis and osteoarthritis show high temperatures
due to inflammation and pain. Enthesiopathies, fibromyalgia, tennis elbow,
Objects with temperatures above absolute zero emit wavelengths in the and muscle spasm and injury also present hot spots and swelling in different
electromagnetic spectrum called infrared radiation [1]. Infrared Thermo- muscles [1,3,4,6,9]. Similarly, the eyes of patients with dry eye syndrome,
graphy (IRT) allows to acquire 2D images of such radiation from a body, Graves ophthalmopathy, and ocular diseases exhibit temperatures higher
which can be used to detect the temperature distribution of objects in real than those of healthy people [1,10–13]. Additionally, the temperature of the
time [2–8]. This is an advantage in the medical field because changes in eyes can be used for fever screening [1,3,9].
body temperature allow to identify physiological variations that are asso- Areas with low temperature (caused by cold stimulation, muscle con-
ciated with various pathologies. In addition, IRT does not induce any risk to traction, and reduced motion) can appear in cases of Raynaud’s phenomenon,
human health, it is non-invasive, low-cost, and portable. carpal tunnel syndrome, thoracic outlet syndrome, long lasting injuries, os-
For instance, the joints of knees, ankles, fingers, and elbows of patients teoarthritis of the hip, and frozen shoulder [3,14–17]. Furthermore, the

Fully documented templates are available in the elsarticle package on CTAN.


Corresponding author.

E-mail addresses: mariahenao191248@correo.itm.edu.co (M.C. Henao-Higuita), alexandrabenitez176383@correo.itm.edu.co (A. Benítez-Mesa),


hermesfandino@itm.edu.co (H. Fandiño-Toro), adrianaguerrero@itm.edu.co (A. Guerrero-Peña), gloriadlondono@itm.edu.co (G. Díaz-Londoño).

https://doi.org/10.1016/j.infrared.2018.10.038
Received 28 February 2018; Received in revised form 17 September 2018; Accepted 30 October 2018
Available online 31 October 2018
1350-4495/ © 2018 Elsevier B.V. All rights reserved.
M.C. Henao-Higuita et al. Infrared Physics and Technology 95 (2018) 203–212

In the above-mentioned cases, temperature differences between


contralateral regions or between healthy people and patients are cal-
culated and used as diagnostic criteria. Furthermore, if the temperature
differences are significant, they are considered a sign and symptom of a
disease. Otherwise, these differences fall within the temperature range
of normal healthy people or measurement uncertainty.
Nonetheless, the emissivity of the human skin changes according to
ethnic characteristics [1,9,22,23] and age[9,22,23]. This indicates that the
thermal patterns of healthy people are specific to each population and,
therefore, they should be established independently. Moreover, maximum
and minimum temperature differences between contralateral regions should
be calculated for each community that exhibits comparable ethnic char-
acteristics.
Some previous studies have established thermal patterns in healthy
Brazilian [9], Finnish [9,24], Portuguese [25], Taiwanese [26], and
Mexican populations [22]. In the case of Colombia, no work about
thermal patterns has been reported. However, as this is a multi-ethnic
nation and the average humidity and temperature change from city to
city, said patterns should be determined in each region of the country.
In order to establish thermal patterns, the segmentation methods should
Fig. 1. Set-up to measure the temperature of healthy people. be properly selected for each Region of interest (ROI) since they can affect the
final thermal results [27]. Anterior and posterior regions of different limbs of
the body have been considered in previous studies on thermal patterns of
healthy people [9,24,26]. The images were segmented using the software of
the thermal cameras, which allows to define circular, rectangular, and square
ROIs; however, these procedures can include background pixels, other ROIs,
or not consider pixels of the ROI under analysis. As a result, average and
standard deviations can change due to these extreme data [28]. Other works
have used Otsu’s method to segment thermal images [29–31]. For example,
Barcelos et al. [31] analyzed thermal images of the lower limbs of soccer
players. However, they combined Otsu’s method with a correction method
because the former has been reported to find inaccurate thresholds in thermal
images with large variances in object and background intensities; thus, er-
roneous segmentation results can be generated [31,32].
This study aims to establish thermal patterns of the population of
Medellín, Colombia, because this information can be used to diagnose
illnesses. Thermal images were acquired from the anterior, posterior,
right, and left side of the entire body, and 24 thermograms were re-
corded. A total of 43 ROIs were defined in each subject, including the
eyes, nose, ears, and mouth. Although these organs were not studied in
previous works about the thermal patterns of healthy adults, they can
be used to evaluate emotions, feelings, and stress [33–36].
The thermal images were segmented using the region-growing (RG)
segmentation method [37] and a grid mask algorithm written in Matlab.
These segmentation methods have not been used in previous works about
the thermal patterns of healthy people. On the other hand, these methods
allow to obtain an accurate definition of anatomical regions and provide
thermal results with small standard deviations. The mean temperature (T )
and standard deviations (SD) of each ROI were calculated, and the nor-
mality in the ROIs was verified by the Shapiro–Wilk test. In addition, Stu-
Fig. 2. Region of interest analyzed in this work for Right (R) and Left (L) side. 1. dent’s t-test and Mann–Whitney U test were applied in the comparison
Forehead. 2. R Eye, 3. L Eye, 4. Nose, 5. R Cheekbone, 6. L Cheekbone, 7. Mouth, 8. between contralateral regions with normal and non normal distributions,
Chin, 9. Neck, 10. R Helix, 11. R Outer ear, 12. L Helix, 13. L Outer ear, 14. R Thorax
respectively. Independent samples were assumed in the statistical analysis,
and abdomen, 15. L Thorax and abdomen, 16. R Shoulder, 17. L Shoulder, 18. R
and IBM SPSS Statistics 24 software was used.
Forearm, 19. L Forearm, 20. R Elbow, 21. L Elbow, 22. R Arm, 23. L Arm, 24. R Wrist,
25. L Wrist, 26. R Palm, 27. R Thumb, 28. R Index, 29. R Middle, 30. R Ring, 31. R
Little or Pinky, 32. L Palm, 33. L Thumb, 34. L Index, 35. L Middle, 36. L Ring, 37. L 2. Materials and methods
Little or Pinky, 38. R Thigh, 39. L Thigh, 40. R Knee, 41. L Knee, 42. R Leg, 43. L Leg.
Thirty-seven healthy people participated in this study [average age:
comparison of temperatures between the affected and non-affected region is 27 ± 5 years, average height: 1.68 ± 0.07 m, average weight:
one of the diagnostic criteria for diseases such as complex regional pain 66.52 ± 9.19 kg, and average Body Mass Index (BMI): 23.43 ± 2.89 kg/
syndrome, localized scleroderma, breast cancer, and diabetes neuropathy m2 ]. The group was composed of 17 females and 20 males who were
[3,18]. In the case of localized scleroderma, a temperature difference over residents of Medellín. The thermograms were acquired using a FLIR
0.5 °C between contralateral regions indicates lesion activity [19,20]. In sport A655SC thermal camera with a long wavelength infrared band (7.5 to
and exercise medicine, the assessment of bilateral asymmetry assumes a re- 14 µ m), a spatial resolution of 640 × 480 pixels, an accuracy of ± 2 °C,
levance to determine potential risks of injury and functional deficits of un- and a NETD under 30 mK. Said camera uses FLIR R&D software 3.3.
healthy athletes and non-athletes [21]. A total of 24 thermograms were recorded from different views (anterior,

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M.C. Henao-Higuita et al. Infrared Physics and Technology 95 (2018) 203–212

Fig. 3. Region-growing segmentation of forehead and neck ROIs. (a) Example of a thermogram. (b) Superimposition of forehead and neck ROIs on the thermogram in (a).

Fig. 4. The grid mask algorithm applied onto the trunk. (a) Example of a thermogram. (b) Superimposition of the grid mask on the thermogram in (a).

posterior, right, and left side) of each person in standing position. During the July 2017. The room (4.36 × 5.20 m2 ) was adapted to prevent sunlight pe-
measurements, men wore boxer shorts and women wore shorts (topless). As netration. The mean distance between the subject and the camera was 2.15 ±
recommended by previous studies, the participants relaxed for 15 min before 0.08 m. This distance (d) was calculated with Eq. (1), which determines the
the measurements were taken. In addition, the subjects could not engage in area (A) required to visualize images with the camera’s field-of-view (FOV).
physical activity or present pain in any part of the body 12 h prior to the The latter is defined by and , which represent the vertical and horizontal
measurements [1,3,24]. The subjects answered a survey that contained ex- aperture angles of the camera lens, respectively (FOV = × ). For the FLIR
clusion criteria such as any illness that could affect skin temperature, other A655SC camera, these values are = 19° and = 25°.
types of alteration in the metabolism (the thyroid or the peripheral nervous
1/2
system), or if they had suffered any bone fracture. The female survey in-
A
cluded additional questions about hormonal cycle (menstrual period) and d=
gynecological conditions and processes such as lactation, myomas, cysts, 4 × tan ( ) × tan ( )
2 2 (1)
polycystic ovaries, and gestation, which served as exclusion criteria for
women. Moreover, participants were instructed to avoid smoking, drinking Additionally, a black wood screen (2.00 × 1.20 ) was designed to
m2
alcohol, and energy and stimulating beverages in order to prevent thermal frame each subject and provide a uniform background in the thermograms;
alterations; they were also informed that skin creams and lotions should not this structure is lightweight and can be easily moved. Fig. 1 shows the geo-
be applied on the skin [28]. All the subjects signed an informed consent metric configuration inside the doctor’s office and the black wood screen.
approved by the Ethics Committee of Instituto Tecnológico Metropolitano
(ITM). 2.2. Acquisition protocol

2.1. Set-up to measure the temperature of healthy people Most of the settings for the acquisition protocol were defined according to
recommendations in previous works [1,3,24,38]. The ambient temperature
All the measurements were carried out in the doctor’s office at ITM in was 25.63 ± 0.35 °C and the relative humidity, 48.76 ± 5.50 %. These

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M.C. Henao-Higuita et al. Infrared Physics and Technology 95 (2018) 203–212

parameters were first measured at different times of the day in order to because the TH threshold guarantees that the segmented regions do not
identify the period that presented the slightest fluctuations. As a result, data include pixels from the background of the thermograms.
were collected in the morning, when the lowest level of fluctuations occurred The function of the grid mask algorithm is to apply a grid that di-
[38]. Temperature and humidity were measured with a hygro-thermometer vides thermograms into square regions, which helps in the segmenta-
and recorded for each acquisition. Based on the results of the reflector tion of comparatively large body regions, such as the trunk and thighs.
method proposed by ASTM standard E1862 [39], in this case the value of Fig. 4 shows the segmentation of the posterior side of the trunk.
reflected temperature was equal to the ambient temperature.
2.4. Statistical methods
2.3. Thermogram processing
In this work, the sample size was determined according to accuracy
A series of codes written in Matlab were programmed for processing the data, which depends on the margin of error (e) and a 95% confidence
acquired thermograms. Additionally, 43 ROIs of each subject were segmented level. Furthermore, the following expression was used to calculate the
(Fig. 2). The segmentation was carried out using the RG segmentation optimum sample size [41–43]:
method [37] and a grid mask algorithm. RG segmentation starts with a pixel
Z12 /2 SD
2
chosen as the seed and a TH value set as the threshold; based on them, n=
e2 (2)
neighboring pixels are added. Finally, the algorithm stops when the differ-
ences between the region’s mean and new pixels are higher than TH [40]. where n is the sample size and Z1 /2 is the value of standard normal dis-
The forehead, eyes, noise, ears, joints, and phalanges were segmented tribution for a 95% confidence level ( = 0.05). In this case, Z0.975 = 1.96.
with this algorithm. Fig. 3 shows the results of the RG segmentation of A pilot experiment with six subjects enabled to calculate the SD of
forehead and neck ROIs. For a better visualization, each ROI is framed by a the temperature(0.4435) and define e as a value lower than 1% of T of
black rectangle whose centroid (white dot) is the corresponding seed pixel. the trunk in the pilot experiment (0.145 °C). At this point, the sample
During the experiments, RG segmentation proved to be a suitable method size was 36 subjects.

Table 1
Mean temperature and standard deviations (T ± SD) in °C and p-values (p) of Shapiro–Wilk test in % of the right (R) and left (L) ROIs under analysis.
View

Region of interest Anterior Right side Left side Posterior

T ± SD p T ± SD p T ± SD p T ± SD p

Forehead 34.56 ± 0.49 7.20 34.58 ± 0.46 7.00 34.54 ± 0.57 5.40 – –
R Eye 34.32 ± 0.37 5.10 34.29 ± 0.56 52.50 – – – –
L Eye 34.32 ± 0.41 25.00 – – 34.09 ± 0.47 78.10 – –
R Cheekbone 33.80 ± 0.62 27.70 34.16 ± 0.73 8.40 – – – –
L Cheekbone 33.75 ± 0.64 63.10 – – 33.91 ± 0.70 27.40 – –
Nose 33.71 ± 1.11 4.20 32.99 ± 1.50 0.20 33.54 ± 0.94 4.20 – –
Mouth 34.36 ± 0.38 15.10 34.34 ± 0.53 56.00 34.09 ± 0.37 87.40 – –
Chin 34.23 ± 0.55 53.30 34.18 ± 0.42 13.30 34.14 ± 0.46 39.30 – –
R Helix – – 31.16 ± 0.67 99.40 – – – –
L Helix – – – – 31.69 ± 0.70 73.50 – –
R Outer Ear – – 34.64 ± 0.50 45.40 – – – –
L Outer Ear – – – – 34.54 ± 0.48 0.47 – –
Neck 34.39 ± 0.52 65.80 34.42 ± 0.50 60.50 34.46 ± 0.58 20.80 34.04 ± 0.61 70.90
R Thorax and Abdomen 33.29 ± 0.82 99.90 32.97 ± 0.88 84.40 – – 33.02 ± 0.92 28.50
L Thorax and Abdomen 33.29 ± 0.83 90.40 – – 32.98 ± 0.87 65.00 33.09 ± 0.97 28.50
R Shoulder 33.54 ± 0.71 93.80 – – – – 32.94 ± 0.78 6.90
L Shoulder 33.53 ± 0.69 75.10 – – – – 32.76 ± 0.76 4.30
R Arm 32.94 ± 0.68 43.50 – – – – 31.72 ± 0.71 94.70
L Arm 32.89 ± 0.70 84.80 – – – – 31.60 ± 0.66 64.70
R Elbow 32.72 ± 0.62 18.70 – – – – 32.19 ± 0.62 6.80
L Elbow 32.64 ± 0.69 2.60 – – – – 32.02 ± 0.62 48.10
R Forearm 32.81 ± 0.64 16.10 32.81 ± 0.62 49.90 32.55 ± 0.53 44.50 32.50 ± 0.51 10.20
L Forearm 32.77 ± 0.66 9.70 32.72 ± 0.64 12.70 32.42 ± 0.59 75.10 32.47 ± 0.56 36.60
R Wrist 32.99 ± 0.75 49.40 32.72 ± 0.69 44.20 32.05 ± 0.93 57.80 32.33 ± 0.87 59.60
L Wrist 32.85 ± 0.75 60.60 32.69 ± 0.69 45.20 31.98 ± 0.86 10.80 32.18 ± 0.82 86.00
R Palm or Back 32.58 ± 1.31 12.90 – – – – 32.26 ± 1.23 15.70
L Palm or Back 32.47 ± 1.27 10.60 – – – – 32.15 ± 1.27 61.80
R Thumb 32.20 ± 1.47 17.40 – – – – 32.22 ± 1.57 1.10
L Thumb 32.24 ± 1.38 7.10 – – – – 32.10 ± 1.65 1.00
R Index Finger 31.83 ± 1.94 2.70 – – – – 32.10 ± 1.71 2.80
L Index Finger 31.83 ± 1.75 1.90 – – – – 32.25 ± 1.48 7.20
R Middle Finger 31.98 ± 1.75 7.80 – – – – 31.96 ± 1.93 1.30
L Middle Finger 31.85 ± 1.78 0.70 – – – – 32.46 ± 1.38 9.40
R Ring Finger 31.63 ± 1.98 6.90 – – – – 32.26 ± 1.65 5.50
L Ring Finger 31.93 ± 1.55 15.50 – – – – 32.17 ± 1.73 0.60
R Pinky 31.23 ± 2.34 1.60 – – – – 31.75 ± 1.92 6.50
L Pinky 31.61 ± 1.87 14.80 – – – – 31.26 ± 2.38 0.60
R Thigh 32.27 ± 0.67 53.20 31.99 ± 0.96 99.70 32.38 ± 0.65 67.60 32.10 ± 0.78 98.60
L Thigh 32.26 ± 0.69 47.90 32.40 ± 0.75 82.10 31.90 ± 0.89 82.40 32.16 ± 0.83 96.70
R Knee 31.39 ± 0.72 71.60 31.78 ± 0.68 45.60 31.75 ± 0.64 96.20 32.40 ± 0.57 26.30
L Knee 31.36 ± 0.76 91.60 31.68 ± 0.69 100.00 31.74 ± 0.71 87.20 32.44 ± 0.60 80.30
R Leg 32.12 ± 0.63 12.00 32.08 ± 0.62 20.70 31.93 ± 0.67 47.40 31.75 ± 0.63 79.10
L Leg 32.08 ± 0.68 73.70 31.90 ± 0.71 38.20 32.13 ± 0.69 11.30 31.81 ± 0.63 28.30

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M.C. Henao-Higuita et al. Infrared Physics and Technology 95 (2018) 203–212

In addition, the authors ensured that the temperature was normally regions under study. In most regions, T varied between 31.16 °C and
distributed; therefore, a sample size above 30 individuals provided a 34.58 °C, but in the external outer ear, forehead, and neck it was over
good estimation of temperature (central limit theorem) [41–44]. 34.54 °C. In the helix, knee, anterior view of the right pinky finger, posterior
Based on the considerations above, 37 healthy people were studied. The view of the left pinky finger, and left arm, it ranged between 31.16 °C and
statistic sampling technique used simple random sampling with a con- 31.60 °C.
fidence level of 0.95 and a sampling error of 0.145 °C; in addition, in- The SDs of all the ROIs were between 0.36 °C and 2.34 °C. The
dependent samples were assumed. The software IBM SPSS Statistics 24 was highest values were found on the nose, hands, and phalanges because
used to analyze the results. T and SD were calculated for each ROI and the these ROIs are acral regions of the body, they are less irrigated by blood
Shapiro–Wilk test [44] was applied to evaluate the normality of the data. than central areas, and such irrigation presents higher variability.
Parametric and non-parametric tests were carried out on contralateral Most regions exhibited a normal distribution because their p-value was
ROIs in order to define temperature differences between the latter. If the ROIs over 5 % , except for the nose, helix, left shoulder, left elbow, and fingers.
exhibited a normal distribution, Levene’s test and Student’s t-test were used to
assess the equality of variances and T , respectively. If the ROIs did not show a 3.2. Analysis of contralateral regions
normal distribution, Mann–Whitney U test [45] was applied to estimate the
equality of T . In all the tests, the significance level was = 0.05. Table 2 shows the results of T and SD of the entire regions, as well as the
parametric and non-parametric tests of the comparison between contralateral
3. Results and discussion ROIs. In addition, the temperature differences between left and right regions
were calculated, TRL . The variances of most contralateral ROIs show no
3.1. Average and standard deviations significant differences. Furthermore, Student’s t-test for equality variance was
applied and the temperature difference was found to be insignificant.
Table 1 shows the results of T , SD, and the p-value normality test (p- Nonetheless, a significant difference between variances was found in the
value) [44] of the anterior, posterior, right, and left lateral views of the eyes. Student’s t-test for unequal variance was applied and the p-values were
Table 2
Mean temperature and standard deviations (T ± SD) in °C and p-values (p) of Student’s t test and Mann–whitney U test in % of the comparison between contralateral
regions, right (R) and left (L).
Parametric and Non-parametric test

Region of interest Student’s t-test Mann–Whitney U test

T ± SD TRL p p

Forehead 34.557 ± 0.512 – 98.900 –


R Eye 34.308 ± 0.473 0.102 ± 0.206 10.800 –
L Eye 34.206 ± 0.432 – – –
R Cheekbone 33.969 ± 0.675 0.123 ± 0.305 16.600 –
L Cheekbone 33.846 ± 0.663 – – –
Nose 33.311 ± 1.454 – – 10.900
Mouth 34.299 ± 0.418 – 22.700 –
Chin 34.193 ± 0.493 – 49.000 –
R Helix 31.392 ± 0.866 0.136 ± 0.367 53.300 –
L Helix 31.256 ± 0.741 – – –
R Outer Ear 34.566 ± 0.494 0.006 ± 0.217 99.000 –
L Outer Ear 34.572 ± 0.459 – – –
Neck 34.278 ± 0.615 – 3.400 –
R Thorax and Abdomen 33.154 ± 0.875 0.038 ± 0.401 75.800 –
L Thorax and Abdomen 33.192 ± 0.886 – – –
R Shoulder 33.179 ± 0.837 0.062 ± 0.384 65.800 –
L Shoulder 33.117 ± 0.847 – – –
R Arm 32.273 ± 0.971 0.103 ± 0.441 52.500 –
L Arm 32.170 ± 0.963 – – –
R Elbow 32.405 ± 0.728 0.116 ± 0.337 34.600 –
L Elbow 32.289 ± 0.751 – – –
R Forearm 32.674 ± 0.619 0.109 ± 0.284 15.400 –
L Forearm 32.565 ± 0.628 – – –
R Wrist 32.342 ± 1.022 0.120 ± 0.465 36.200 –
L Wrist 32.222 ± 1.019 – – –
R Palm and Back 32.417 ± 1.273 0.113 ± 0.580 – 59.100
L Palm and Back 32.304 ± 1.273 – – –
R Thumb 32.211 ± 1.509 0.025 ± 0.680 – 90.300
L Thumb 32.186 ± 1.476 – – –
R Index Finger 31.887 ± 1.908 0.169 ± 0.800 – 79.700
L Index Finger 32.056 ± 1.590 – – –
R Middle Finger 31.966 ± 1.827 0.136 ± 0.787 – 85.800
L Middle Finger 32.102 ± 1.622 – – –
R Ring Finger 31.934 ± 1.839 0.116 ± 0.792 – 82.300
L Ring Finger 32.050 ± 1.633 – – –
R Pinky 31.481 ± 2.149 0.056 ± 0.978 – 87.200
L Pinky 31.425 ± 2.142 – – –
R Thigh 32.182 ± 0.782 0.002 ± 0.361 98.400 –
L Thigh 32.184 ± 0.802 – – –
R Knee 31.828 ± 0.744 0.022 ± 0.350 80.900 –
L Knee 31.806 ± 0.790 – – –
R Leg 31.966 ± 0.647 0.013 ± 0.361 86.700 –
L Leg 31.979 ± 0.683 – – –

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Table 3
Mean temperature and standard deviation (T ± SD) in °C of the right (R) and left (L) ROIs of the populations of Medellín, Brazil, and Taiwan. The control group is
composed of females and males from Medellín, and the young group is comprised of Taiwanese people aged between 20 and 60.
Medellín Brazil Medellín Brazil Medellín Taiwan

Region of interest Female (n = 17) Female (n = 117) Male (n = 20) Male (n = 103) Control (n = 37) Young (n = 37)

T ± SD T ± SD T ± SD T ± SD T ± SD T ± SD

R Arm 32.66 ± 0.86 28.40 ± 2.20 33.07 ± 0.63 28.17 ± 2.61 – –


L Arm 32.63 ± 0.88 28.60 ± 2.20 32.99 ± 0.67 28.34 ± 2.62 – –
R Forearm 32.56 ± 0.77 30.39 ± 1.20 32.67 ± 0.50 30.75 ± 1.20 32.81 ± 0.64 31.70 ± 0.50
L Forearm 32.54 ± 0.89 30.59 ± 1.20 32.85 ± 0.62 30.96 ± 1.10 32.77 ± 0.66 31.60 ± 0.60
Anterior R Thigh 32.07 ± 0.47 28.62 ± 1.30 32.46 ± 0.78 29.70 ± 1.10 32.27 ± 0.67 32.20 ± 0.60
L Thigh 32.04 ± 0.62 28.72 ± 1.30 32.48 ± 0.71 29.75 ± 1.20 32.26 ± 0.69 32.20 ± 0.60
R Leg 32.00 ± 0.56 30.18 ± 1.20 32.21 ± 0.69 30.21 ± 1.40 32.12 ± 0.63 30.30 ± 0.80
L Leg 31.96 ± 0.52 30.11 ± 1.20 32.18 ± 0.79 30.19 ± 1.40 32.08 ± 0.68 30.40 ± 0.60
R Palm – – – – 32.58 ± 1.31 31.80 ± 1.10
L Palm – – – – 32.47 ± 1.27 31.40 ± 1.30

R arm 31.35 ± 0.81 28.59 ± 1.40 31.95 ± 0.64 29.36 ± 1.20 – –


L Arm 31.30 ± 0.79 28.48 ± 1.40 31.63 ± 0.53 29.22 ± 1.20 – –
R Forearm 32.45 ± 0, 69 30.20 ± 1, 20 32.67 ± 0.50 30.61 ± 1.10 32.50 ± 0.51 31, 00 ± 0.60
L Forearm 32.35 ± 0.77 29.95 ± 1.10 32.46 ± 0.46 30.30 ± 1.10 32.47 ± 0.56 30.50 ± 0.60
Posterior R Thigh 31.62 ± 0.90 29.26 ± 1.10 32, 60 ± 0.71 30.28 ± 1.10 32.10 ± 0.78 30.30 ± 0.60
L Thigh 31.71 ± 0.68 29.15 ± 1.10 32.52 ± 0.66 30.20 ± 1.20 32.16 ± 0.83 30.30 ± 0.70
R Leg – – – – 31.75 ± 0.63 29.90 ± 0.70
L Leg – – – – 31.81 ± 0.63 29.90 ± 0.70
R Dorsal Hand – – – – 32.26 ± 1.23 30.80 ± 0.70
L Dorsal Hand – – – – 32.15 ± 1.27 30.50 ± 0.60

over 5%, which indicates no significant difference in the T of the eyes. these aspects. The collected images enabled to determine the temperature
Moreover, significant differences between T were found in the neck, because value of 43 regions located throughout the body. Besides, statistical tests
the blood irrigation in lateral regions is higher than in anterior-posterior allowed to establish that the contralateral areas present a normal distribution,
areas. equal variance, and no significant differences, which makes such regions
Mann–Whitney U test was used to evaluate the equality of T in the useful for the medical diagnosis of pathologies that affect thermal patterns.
regions that did not show a normal distribution, and no significant In order to correctly evaluate anatomically complex regions, such as
differences between T were found. the hands or ears, their sections should be considered separately (e.g.,
phalanges, back of hand, auricle of the external auditory canal) due to
3.3. Comparison with previous works their variable thermal behavior.
RG segmentation and the grid mask algorithm were essential for this
The results obtained in this work were compared with those re- study because they allowed to obtain, in a quick and effective way, data
ported by Marins et al. [9] and Niu et al. [26], who determined thermal from the areas under analysis. With the aim of properly and more
patterns of upper and lower limbs of healthy Brazilian and Taiwanese precisely selecting ROIs, future studies should implement software or
people, respectively. Their methods and environmental conditions are programming algorithms to automatically segment the image, as this
similar to those described in this study. In this work, the temperature of would enable to acquire more accurate thermal data.
the limbs varied between 31.30 °C and 33.07 °C; in Brazil, between The method implemented in this study should be replicated in future
28.17 °C and 30.61 °C [9]; and in Taiwan, between 30.30 °C and works in other areas of Colombia where different ethnic characteristics are
32.77 °C [26]. Therefore, the temperature range of the population of found in order to obtain the thermal patterns of each region.
Medellín is higher than that of individuals in Brazil and Taiwan. Finally, to determine a thermal difference that indicates a patho-
Student’s t-test was applied to the comparison of temperatures logical behavior, it is necessary to establish a significant difference in
among young adults in the three cases: Medellín, Brazil, and Taiwan. each ROI using both parametric and non-parametric tests, which can be
Table 3 shows the T and SD of this comparison. Significant differences further developed in future works.
between populations were found due to the fact that the p-values were
below 5%. Such differences can be explained by the skin type of each Conflict of interest
population and atmospheric conditions. These results reveal the need to
establish thermal patterns for each population. The authors declared that there is no conflict of interest.

4. Conclusions and recommendations Acknowledgments

Conditions such as the technical characteristics of the camera and en- This work was supported by Instituto Tecnológico Metropolitano
vironmental and individual factors were essential to define the acquisition (ITM). Additionally, the authors would like to thank the medical service
protocol, since the quality of the images that were obtained depended on at ITM and the participants in this study.

Appendix A. Region of interest

This Appendix contains the thermograms and ROIs under analysis.


See Figs. A.1–A.4.

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Fig. A.1. Region-growing and grid mask algorithm segmentation of two ROIs: leg and thigh.

Fig. A.2. Region-growing segmentation of the ROIs of the arm.

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Fig. A.3. Region-growing segmentation of the ROIs of the hand.

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Fig. A.4. Region-growing segmentation of the ROIs of the head.

References [5] N. Fett, V.P. Werth, Update on morphea: Part II. outcome measures and treatment,
J. Am. Acad. Dermatol. 64 (2) (2011) 231–242.
[6] F.E. Ring, K. Ammer, Infrared thermal imaging in rheumatic diseases: a biblio-
[1] B. Lahiri, S. Bagavathiappan, T. Jayakumar, J. Philip, Medical applications of in- graphic overview, Thermol. Intern. 11 (2001) 161–167.
frared thermography: a review, Infrared Phys. Technol. 55 (4) (2012) 221–235. [7] D.L. Balageas, Termografía infrarroja: una técnica multifacética para la evaluación
[2] P.C. Zancanaro, A.R. Isaac, L.T. Garcia, I.M. Costa, Esclerodermia localizada na no destructiva (end), in: IV Conferencia Panamericana de END, Buenos Aires,
criança: aspectos clínicos, diagnósticos e terapêuticos, An Bras Dermatol. 84 (2) AAENDE, 2007, pp. 1–14.
(2009) 161–172. [8] D. Formenti, N. Ludwig, A. Rossi, A. Trecroci, G. Alberti, M. Gargano, A. Merla,
[3] E. Ring, K. Ammer, Infrared thermal imaging in medicine, Physiol. Meas. 33 (3) K. Ammer, A. Caumo, Skin temperature evaluation by infrared thermography:
(2012) R33. comparison of two image analysis methods during the nonsteady state induced by
[4] M.L. Brioschi, L.T. Yeng, E.M.H. Pastor, M.J. Teixeira, Infrared imaging use in physical exercise, Infrared Phys. Technol. 81 (2017) 32–40.
rheumatology, Revista Brasileira de Reumatol. 47 (1) (2007) 42–51. [9] J.C.B. Marins, A.A. Fernandes, S.P. Cano, D.G. Moreira, F.S. da Silva, C.M.A. Costa,

211
M.C. Henao-Higuita et al. Infrared Physics and Technology 95 (2018) 203–212

I. Fernandez-Cuevas, M. Sillero-Quintana, Thermal body patterns for healthy bra- M.Á. García-Concepción, M. Sillero-Quintana, Classification of factors influencing
zilian adults (male and female), J. Thermal Biol. 42 (2014) 1–8. the use of infrared thermography in humans: A review, Infrared Phys. Technol. 71
[10] J.-H. Tan, E. Ng, U.R. Acharya, C. Chee, Infrared thermography on ocular surface (2015) 28–55.
temperature: a review, Infrared Phys. Technol. 52 (4) (2009) 97–108. [29] R. Koprowski, Automatic analysis of the trunk thermal images from healthy subjects
[11] J.-H. Tan, E. Ng, U.R. Acharya, C. Chee, Study of normal ocular thermogram using and patients with faulty posture, Comput. Biol. Med. 62 (2015) 110–118.
textural parameters, Infrared Phys. Technol. 53 (2) (2010) 120–126. [30] C.B. Pereira, X. Yu, M. Czaplik, V. Blazek, B. Venema, S. Leonhardt, Estimation of
[12] U. Brunsmann, U. Sauer, S. Arba-Mosquera, T. Magnago, N. Triefenbach, Evaluation breathing rate in thermal imaging videos: a pilot study on healthy human subjects,
of thermal load during laser corneal refractive surgery using infrared thermo- J. Clin. Monit. Comput. (2016) 1–14.
graphy, Infrared Phys. Technol. 53 (5) (2010) 342–347. [31] E.Z. Barcelos, W.M. Caminhas, E. Ribeiro, E.M. Pimenta, R.M. Palhares, A combined
[13] T.-C. Chang, Y.-L. Hsiao, S.-L. Liao, Application of digital infrared thermal imaging method for segmentation and registration for an advanced and progressive eva-
in determining inflammatory state and follow-up effect of methylprednisolone pulse luation of thermal images, Sensors 14 (11) (2014) 21950–21967.
therapy in patients with graves’ ophthalmopathy, Graefe’s Arch. Clin. Exp. [32] M. Etehadtavakol, E. Ng, N. Kaabouch, Automatic segmentation of thermal images
Ophthalmol. 246 (1) (2008) 45–49. of diabetic-at-risk feet using the snakes algorithm, Infrared Phys. Technol. 86
[14] K. Ammer, B. Engelbert, E. Kern, The determination of normal temperature values (2017) 66–76.
of finger joints, Thermol. Int. 12 (2002) 23. [33] E. Salazar-López, E. Domínguez, V.J. Ramos, J. de la Fuente, A. Meins, O. Iborra,
[15] R. KANIE, Thermographic evaluation on osteoarthritis of hip, Biomed. Thermol.: J. G. Gálvez, M. Rodríguez-Artacho, E. Gómez-Milán, The mental and subjective skin:
Japanese Soc. Thermorogy. 15 (2) (1997) 72–76. Emotion, empathy, feelings and thermography, Conscious. Cognit. 34 (2015)
[16] P. Vecchio, A. Adebajo, M. Chard, P.P. Thomas, B. Hazleman, Thermography of 149–162.
frozen shoulder and rotator cuff tendinitis, Clin. Rheumatol. 11 (3) (1992) [34] A. Di Giacinto, M. Brunetti, G. Sepede, A. Ferretti, A. Merla, Thermal signature of
382–384. fear conditioning in mild post traumatic stress disorder, Neuroscience 266 (2014)
[17] K. Ammer, B. Engelbert, S. Hamerle, E. Kern, S. Solar, K. Kuchar, Thermography of 216–223.
the painful shoulder, Eur. J. Thermol 8 (1998) 93–100. [35] B.R. Nhan, T. Chau, Classifying affective states using thermal infrared imaging of
[18] O. Faust, U.R. Acharya, E. Ng, T.J. Hong, W. Yu, Application of infrared thermo- the human face, IEEE Trans. Biomed. Eng. 57 (4) (2010) 979–987.
graphy in computer aided diagnosis, Infrared Phys. Technol. 66 (2014) 160–175. [36] V. Engert, A. Merla, J.A. Grant, D. Cardone, A. Tusche, T. Singer, Exploring the use
[19] G. Martini, K. Murray, K. Howell, J. Harper, D. Atherton, P. Woo, F. Zulian, of thermal infrared imaging in human stress research, PloS one 9 (3) (2014)
C. Black, Juvenile-onset localized scleroderma activity detection by infrared ther- e90782.
mography, Rheumatology 41 (10) (2002) 1178–1182. [37] M.M.S.J. Preetha, L.P. Suresh, M.J. Bosco, Image segmentation using seeded region
[20] K.J. Howell, A. Lavorato, M.T. Visentin, R.E. Smith, G. Schaefer, C.D. Jones, growing, 2012 International Conference on Computing, Electronics and Electrical
L. Weibel, C.P. Denton, J.I. Harper, P. Woo, Validation of a protocol for the as- Technologies (ICCEET), IEEE, 2012, pp. 576–583.
sessment of skin temperature and blood flow in childhood localised scleroderma, [38] J.C.B. Marins, D. Formenti, C.M.A. Costa, A. de Andrade Fernandes, M. Sillero-
Skin Res. Technol. 15 (3) (2009) 346–356. Quintana, Circadian and gender differences in skin temperature in militaries by
[21] A. Trecroci, D. Formenti, N. Ludwig, M. Gargano, A. Bosio, E. Rampinini, G. Alberti, thermography, Infrared Phys. Technol. 71 (2015) 322–328.
Bilateral asymmetry of skin temperature is not related to bilateral asymmetry of [39] E. Bauer, V.P. De Freitas, N. Mustelier, E. Barreira, S.S. de Freitas, Infrared ther-
crank torque during an incremental cycling exercise to exhaustion, PeerJ 6 (2018) mography–evaluation of the results reproducibility, Struct. Survey 33 (1) (2015)
e4438. 20–35.
[22] E.S. Kolosovas-Machuca, F.J. González, Distribution of skin temperature in mexican [40] Z. Wang, G. Yu, Y. Kang, Y. Zhao, Q. Qu, Breast tumor detection in digital mam-
children, Skin Res. Technol. 17 (3) (2011) 326–331. mography based on extreme learning machine, Neurocomputing 128 (2014)
[23] K. Ammer, D. Formenti, Does the type of skin temperature distribution matter? 175–184.
Thermol. Int. 26 (2) (2016) 51–54. [41] S. Larsen, M. Osnes, W. Eidsaunet, L. Sandvik, Factors influencing the sample size,
[24] N. Zaproudina, V. Varmavuo, O. Airaksinen, M. Närhi, Reproducibility of infrared exemplified by studies on gastroduodenal tolerability of drugs, Scandinavian J.
thermography measurements in healthy individuals, Physiol. Meas. 29 (4) (2008) Gastroenterol. 20 (4) (1985) 395–400.
515. [42] P. Kadam, S. Bhalerao, Sample size calculation, Int. J. Ayurveda Res. 1 (1)
[25] R. Vardasca, E. Ring, P. Plassmann, C. Jones, Thermal symmetry of the upper and (2010) 55.
lower extremities in healthy subjects, Thermol. Int. 22 (2) (2012) 53–60. [43] A. Kirby, V. Gebski, A.C. Keech, Determining the sample size in a clinical trial, Med.
[26] H.-H. Niu, P.-W. Lui, J.S. Hu, C.-K. Ting, Y.-C. Yin, Y.-L. Lo, L. Liu, T.-Y. Lee, J. Australia 177 (5) (2002) 256–257.
Thermal symmetry of skin temperature: normative data of normal subjects in [44] J.L. Devore, Probabilidad y estadística para ingenierías y ciencias, Cengage
taiwan, Chinese Med. J.-Taipei- 64 (8) (2001) 459–468. Learning Editores, 2008.
[27] E. Ring, K. Ammer, B. Wiecek, P. Plassmann, C. Jones, A. Jung, P. Murawski, [45] I. Pedrosa, J. Juarros-Basterretxea, A. Robles-Fernández, J. Basteiro, E. García-
Quality assurance for thermal imaging systems in medicine, Thermol. Int. 17 (3) Cueto, Pruebas de bondad de ajuste en distribuciones simétricas,¿ qué estadístico
(2007) 103–106. utilizar? Univ. Psychol. 14 (1) (2015) 245–254.
[28] I. Fernández-Cuevas, J.C.B. Marins, J.A. Lastras, P.M.G. Carmona, S.P. Cano,

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