1. INTRODUCTION
In veterinary medicine, one of the major routine tests
performed as a physical examination of animals is measuring their body
temperature (Goodwin, 1998). In farm animals, such as sheep and goats, it is a
possible indicator of early disease detection (Fuchs et al., 2019).
Animals’ body temperature increases when they suffer stress or diseases; for
example, foot and mouth disease and mastitis (Arfuso et al., 2022), as
well as during some painful husbandry procedures like ear tagging (Zebaria et
al., 2021).
As a standard practice of measuring the temperature of the
animal’s body, rectal thermometers are used, mainly because it is inexpensive.
However, it has some limitations as it is an invasive method and needs to
restrain animals so the animals might be stressed and the readings might be
abnormal (Soerensen and Pedersen, 2015). In addition, diseases can be
transmitted through this method of rectal thermometry when measuring the
temperature of larger groups of animals (Katsoulos et al., 2016).
Over the last two decades, the infrared thermal imaging
(IRT) technique as a new and non-invasive method has been widely used in
research regarding farm animals such as sheep and cattle (Knízková et al.,
2007; George et al., 2014). The purpose of IRT is to early detection of
stress, and heat stress and minimize the errors in temperature measurement as
it is a non-invasive method (Cai et al., 2023). When an animal is in a
stressful state, the hypothalamus pituitary adrenal axis is activated to
stimulate the release of adrenal steroids and catecholamines; thus, an animal’s
heat can be lost and is detected by the decreasing surface temperatures
(Proctor and Carder, 2016; McManus et al., 2016; Weaver et al.,
2021).
Since the surface temperature of an animal changes during
abnormal environments such as illness, and stress; the core body and the
infection site temperatures are increased while the peripheral temperature is
decreased (Hussein and Al-Naqshabendy, 2024a).
That is mainly because of the vasoconstriction of the
surface blood vessels and vasodilation of the infected region of the body
(Molony et al., 2012). Therefore, this method may accurately detect
changes in the thermal status of an animal’s body while reducing labor costs
and fewer errors (Cai et al., 2023). The researchers used different body
regions to measure surface temperature, including eyes, ears, nostrils, udder,
hooves, and neck (McManus et al., 2016). This method has been used to
measure positive, and negative emotions and pain caused by diseases like
mastitis and foot rot in sheep and goats (McLennan et al., 2016; Hussein
and Al-Naqshabendy, 2023, 2024a). There is little information regarding the
correlation and variation in the temperature of the animal’s body between
rectal thermometers and IRT using infrared (IR) cameras and thermometers
(Ibáńez et al., 2023). Therefore, the main purpose of this research was
to assess the precision of the IR cameras and thermometers in measuring
different body regions of sheep.
2. MATERIALS
AND METHODS
Animals And Study Area
This study was undertaken in the Animal Farm of the College
of Agricultural Engineering Sciences, University of Duhok, Kurdistan Region of
Iraq in July and August, 2024. Twenty healthy, 10 Awassi and 10 Karadi ewes,
aged 2 – 4 years, participated in this experiment.
Ethical Statement
All the
procedures for measuring the body temperatures of studied animals were routine
health procedures; thus, the animals were not mistreated or abused. Therefore,
the Animal Ethics Committee of the College of Sciences, University of Zakho,
Kurdistan Region of Iraq ethically approved the research methods with a code of
AEC – 028.
Temperature Data Collection
The focal
sampling was used to collect temperature data individually. Data were collected
twice in a week from 9 to 11 a.m. Each animal was restrained and kept still for
five minutes to eliminate the stress that might be caused by restraining. After
that, the temperature was measured from the rectum using a digital thermometer.
At the same time, the peripheral temperatures were measured from the ears,
muzzle, inner thigh, inguinal region, rectum, vulva, and five areas of the
eyes, including nasal conjunctiva (NC), nasal limbus (NL), center cornea (CC),
temporal limbus (TL) and temporal conjunctiva (TC) using IR thermometer and IR
camera (FLIR E4). The IR data were measured from a distance of 0.5 m, except
for the eye areas, which were collected from a distance of 0.2 m.
Data Analysis
All the
collected temperature data were saved in the new Excel spreadsheet. Then, they
were analyzed using the GenStat Software Program (17th edition, VSN
International). Data were checked for normality; thus, boxplots confirmed by
the Shapiro-Wilk normality test revealed that the temperature data were
normally distributed. Thus, they were analyzed using a one-way ANOVA test
followed by Fisher’s Unprotected LSD test for post hoc comparisons. The Pearson
correlation test was used to find the correlation between the temperatures.
Unless otherwise stated, data were set as mean ± standard error of the mean,
and all the comparisons were stated as significant at P<0.05.
3. RESULTS
Eye Temperature
There were
significant differences (P<0.05) found between the five selected areas of
the eyes measured with the IR thermometer in comparison to rectum and vulva
temperatures measured with the digital thermometer. The temperatures obtained
from the IR thermometer were higher than those obtained from the digital
thermometer collected from the rectum and vulva (Figure 1). The average
temperature for NC, NL, CC, TL, TC, rectum, and vulva were 41.9 ± 0.2, 41.7 ±
0.1, 41.2 ± 0.1, 41.3 ± 0.2, 41.1 ± 0.2, 39.7 ± 0.1, and 39.5 ± 0.1 ℃,
respectively.
Figure 1: Comparison
between five eye areas using an IR thermometer with rectal and vulva
temperature. Note: different letters mean significant differences.
According to
Figure 2, only NC temperature was found to be significantly (P<0.05) higher
than other eye regions, and rectal and vulva temperatures. IR thermal camera
showed no significant differences in the eyes' NL, CC, TL, and TC regions
compared to rectum and vulva temperatures using the digital thermometer (Figure
2). The average temperatures for NC, NL, CC, TL, TC, rectum, and vulva were
40.4 ± 0.1, 39.6 ± 0.2, 39.8 ± 0.1, 39.8 ± 0.1, 39.4 ± 0.2, 39.7 ± 0.1, and
39.5 ± 0.1 ℃, respectively.
Figure 2: The
temperature of five selected eye regions using an IR thermal camera in
comparison to rectal and vulva temperatures using the digital thermometer.
Note: different letters mean significant differences.
the average eye
temperatures using an IR thermometer and IR thermal camera from all selected
regions of the eye in comparison to the rectum and vulva temperatures are shown
in Figure 3. The mean eye temperature of all selected areas of the eyes using
an IR thermometer (41.5 ± 0.1 ℃) was higher significantly than the eye
temperature measured with FLIR IR thermal camera (39.8 ± 0.1 ℃), and
rectum (39.7 ± 0.1 ℃) and vulva (39.5 ± 0.1 ℃) temperatures using
the digital thermometer (Figure 3).
_files/image003.png)
Figure 3: The mean
temperature of all selected eye regions compared with rectal and vulva
temperatures. Note: different letters mean significant differences. EYE-flir is
the eye temperature using an IR camera, EYE-thermometer is the eye temperature
using the IR thermometer, and REC and VUL are rectum and vulva temperatures,
respectively.
The descriptive
statistic data collected from both Karadi and Awassi breeds are shown in Table
1. The minimum temperature was 38.6 ℃ of TC in Karadi sheep using the
FLIR thermal camera, whereas the maximum temperature was 43.6 ℃ in Awassi
sheep using an IR thermometer.
Data obtained from the
Pearson correlation test found that the correlation between rectum temperatures
measured with the FLIR thermal camera and digital thermometer was 0.98, while
the correlation between the digital and IR thermometer was weak, which was
0.38. whereas for vulva temperatures, a strong correlation between FLIR thermal
camera and digital thermometer was found which was 0.79, while the relation
between digital and IR thermometers was 0.06.
4. DISCUSSION
The IR thermal
camera was highly correlated with a digital thermometer, whereas the IR
thermometer was not. Measuring both rectal and vaginal in addition to the eye
temperature using IRT is crucial for animal husbandry and research as the
animal is not restricted and the temperature is correctly detected.
The Pearson correlation
coefficient between rectal temperatures detected by the IR camera and the
digital thermometer was extremely high at 0.98. This high correlation suggests
that the IR camera and the digital thermometers provide relatively close temperature
readings for rectal temperature measurement. This close agreement agrees with
the high accuracy predicted by digital thermometers for measuring the core body
temperature (Pecoraro et al., 2021), and the ability of the IR camera to
capture precise temperature readings as a non-invasive instrument, providing
that it is correctly calibrated and used under suitable conditions. Due to their
reliability, IR thermography cameras are widely used in animal research to
detect diseases such as mastitis and foot rot, stress, and positive affective
states such as stroking ewe’s body, and to detect ovulation time in oestrus
cycles (Arfuso et al., 2022; Ozaki et al., 2024; Hussein and
Al-Naqshabendy, 2023, 2024b).
In contrast,
the correlation between the digital and IR thermometer for measuring the rectal
temperature was not strong, at 0.38. This lower correlation can indicate an
inconsistency between these two types of instruments. IR thermometers are
usually less reliable for measuring core body temperatures since they are not
designed for core body temperature measurement (Pecoraro et al., 2021).
This agrees with the results of Niven et al. (2015) and Sullivan et
al. (2021) who stated that IR thermometers are inaccurate in clinical
conditions and should not be relied on. This limitation possibly explains the
weak correlation between the IR and digital thermometer.
Regarding the vulva's
temperature, the correlation between the camera and the digital thermometer was
high, which was 0.79. This can indicate that both instruments provide
dependable measurements for vulva temperatures, even though they are not as
closely correlated as the rectal temperature. However, the correlation between
the digital and IR thermometer for vulva temperature was low, only 0.06. This
recommends that the 2 instruments provide largely unequal readings for vaginal
temperature. The IR thermometer, principally designed for superficial
temperature measurements, can be affected by ambient temperature or emissivity
settings, contributing to its lower correlation with digital thermometers
(Crawford et al., 2006). The high correlation found between the IR
camera and the digital thermometer for rectal and vaginal temperatures can
recommend that these devices are consistent and can be used interchangeably for
measuring accurate temperature.
This study measured
five different regions of the sheep's eyes, all areas were found to have higher
temperatures significantly than rectal and vulva temperatures using the IR
thermometer, whereas only NC was higher than rectum and vulva temperatures using
the IR camera. The mean eye temperature from the IR camera was similar to those
of the rectum and vulva (Figure 3). This indicates that the eye temperature is
a dependable region for measuring the sheep body temperature using the IRT of
all the five measured regions except NC.
Future research should consider
the explanations behind the lower correlation between IR thermometer and digital
thermometer devices. Several factors such as calibration, environmental
conditions, and the inherent limitations of IR thermometers in capturing
accurate core body temperatures might be explored. Moreover, standardizing the
emissivity settings and measurement protocols for IR thermometer may improve
their consistency and correlation with other thermometer devices.
CONCLUSION
It can be
concluded, according to the results obtained, that IR thermal camera is a
suitable alternative to digital thermometers. Digital thermometers, while
providing the most accurate data, can be invasive and may cause stress to the
animal, particularly when used rectally. Thus, thermal cameras as a
non-invasive and correct method can be an alternative measuring method. Eye and
IT regions can be used to detect core body temperature in ewes.
Acknowledgments
The authors
would like to thank Animal Farm of the Department of Animal Science, College of
Agricultural Engineering Sciences, University of Duhok.
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