Infrared thermography on animal livestock

Infrared thermography has become increasingly promising in veterinary medicine, for being a non-invasive method for detecting body thermal variation. The objective of this review was to elucidate some applications of infrared thermography and its importance on animal livestock. This tool can substitute conventional techniques for diagnosing diseases, inflammation and fever. The body temperature is an important indicator to diagnostics and to understanding physiological aspects due to the close relation between abnormal temperatures and inflammatory processes. Also, it can help monitor reproductive performance and identify more efficient animals, among other purposes. The measurement of infrared temperature allows identifying sick animals, before the appearance of clinical symptoms, making treatment and isolation faster and more accurate, enhancing the profitability and sustainability of the system. However, this tool has some limitations, such as the animal species and environmental factors. Thus, further studies are needed for the application of the thermographic on animal livestock.


Infrared light was discovered by the German astronomer, naturalized English, Sir
William Herschel in the year 1800 after carrying out several experiments, which led to the discovery of thermal radiation, later called infrared light or infrared radiation (Ricca, 2013). Infrared thermography (IRT) is a non-invasive tool that allows the remote measurement of the surface temperature of an animal (Castells et al., 2019), emitted as thermal radiation (Sathiyabarathi et al., 2016;Lowe et al., 2019).
The principle of IRT is that every object with a temperature above absolute zero emits thermal radiation to the environment, in all wave lengths of the infrared spectrum (Poikalainen et al., 2012). The radiation is captured and recorded by a thermal imaging camera that creates a color thermal image, and each color corresponds to a specific temperature (Redaelli and Caglio, 2013). The thermographic image presents a color scale that varies from cold (green and blue) to hot (yellow, orange, red and white) (Castells et al., 2019). Currently, there are several thermal camera models used in animal studies, Table 1. IRT can identify metabolic changes through of the temperature variations in body surface, due to the blood flow variations and tissue metabolic rate (Eddy et al., 2001;Berry et al., al., 2003;Martins et al., 2013;Ludwing et al., 2013).
The IRT can be applied in all animal classes and species, however, anatomical, morphological, metabolic, and physiological differences must be considered . The use of IRT in large animals and large herds has become a useful tool in the preventive diagnosis of several metabolic changes, due to its ability to detect heat variations on the body surface caused by inflammatory processes (Ludwig, 2013).
Moreover, IRT makes it easier to monitor herd health because it does not require direct contact with animals . Also, it allows the adaptation of ethical and sustainable management methods that can be applied in farms, monitoring the herds without stress for the animals. Therefore, IRT can improve the productivity and profitability of different production systems (Neethirajan et al., 2017).
Diseases and heat stress are limiting factors that compromise the productivity of herds and the supply of animal protein to human food, resulting in economic losses.
Disease detection is often expensive and time-consuming (Neethirajan et al., 2017), demanding skilled labor. Body temperature is an important indicator for diagnosing diseases and understanding physiological parameters in animals (Poikalainen et al., 2012;Nääs et al., 2014). Each region of the animal body has a different temperature due to physiological variations, which can help the clinical assessment of these areas (Deak et al., 2019).
Therefore, the objective of this review is to present some applications of infrared thermography and its importance for animal production. We searched for papers in highimpact scientific journals that addressed the use of IRT in diseases diagnosis, inflammatory processes, reproductive monitoring, semen quality, animal efficiency, animals' adaptation, aid to selection, heat stress, and animal welfare.

USE OF INFRARED THERMOGRAPHY IN FARM ANIMALS
The first record of IRT in veterinary medicine was in 1963 in horses. Observing the promising results of IRT in the diagnosis of diseases in humans, the researcher Smith Wendell sought to know the possible applications of IRT in detecting the thermal variation of horses with injured hocks and with calcium deposits in the limbs (Smith, 1964). Over the years, IRT has been widely used in livestock production to register the surface temperature variations in the animals, emitted as infrared radiation, (Sathiyabarathi et al., 2016;McManus et al., 2016;Loyau et al., 2016, Castells et al., 2019. According to Chacur et al. (2018), the IRT is an easy technique to be applied, allowing to perform diagnostic imaging on different body regions, without stress to the animals during the measurements. Castells et al. (2019) related that, as well as ultrasonography, radiography and computed tomography, the infrared thermography is non-invasive tool useful to diagnose diseases. Furthermore, it is a useful tool that helps to understand the interactions between organisms and animal production systems (Eddy et al., 2001;Berry et al., 2003;Ludwig et al., 2013), and there are several applications in livestock production, Table 2.

Bovine
The detection of diseases using IRT can be used in a population of individuals where monitoring can be continuous or repeated, i.e. temperature detection can be performed in a group of animals or among individuals in the group. Lowe et al. (2019) evaluated the association between body thermography and neonatal diarrhea in calves and identified significant changes in the flank and shoulder surface temperatures before the onset of clinical symptoms of the disease. According to these authors, the decrease of temperature of these regions may be due to reduced food intake and metabolic activity caused by disease. Schaefer et al. (2012) evaluating the alterations of the body temperature in calves, reported a relation between the increase of body and eye temperatures and respiratory disease.
Mastitis is an inflammation of the mammary gland caused by several microorganisms, resulting in big economic losses to milk production due to alterations of physical, chemical and bacteriological characteristics of milk (Radostits et al., 2009). The onset of mastitis presents an inflammatory response associated with a rise in temperature in the affected region of the udder (Berry et al., 2003). Research showed that the IRT can identify thermal variations in the mammary gland surface due to increased blood flow in the affected region, Figure 1 (Eddy et al., 2001;Berry et al., 2003;Martins et al., 2013). of dermatitis in dairy cows, showed significant difference in temperature between lame and healthy hooves. Alsaaod et al. (2014) showed that the surface temperature of crown and hoof in dairy cows with digital dermatitis was 2.56°C and 2.49°C, respectively, higher than temperature of crown and hoof in healthy cows.
The standard method of counting parasites on cows and bulls requires a lot of time, work and attention to obtain an accurate result (Fraga et al., 2003;Fraga et al., 2005). A study using IRT, Cortivo et al. (2016) compared the standard method of counting tick and horn flies in cattle raised on pasture with an automatic counting program combined with infrared images. The authors reported that the IRT was efficient and accurate when compared to visual counting. According to those authors, these parasites have a lower temperature than the animals, being easily captured by thermal images ( Figure 2). Source: Cortivo et al. (2016, p. 415) Research have evaluated the ability of the IRT to identify heat stress in cattle and the best anatomical region that would indicate this situation. Mammals can maintain a constant body temperature in several environmental conditions, however when body temperature is above normal, these organisms do not function properly (Hansen, 2013). Daltro et al. (2017) showed that the IRT allowed to show that purebred Holstein cows are less heat tolerant when compared to crossbred Holstein cows, and that the mammary gland would be the ideal anatomical region to find heat stressed animals. Cardoso et al. (2015) recorded differences on the body surface temperature between several Zebu breeds (Gir, Girolanda, Nellore, Indubrasil and Sindhi). The study showed that the temperatures were significantly influenced by environmental factors.
Moreover, the morphometry, coat and skin color traits affected the skin surface temperature, rectal temperature, physiological parameters, and thermal regulation. The study also reported that the Gir breed was the least adapted to the climatic conditions, while the Girolanda and Sindhi breeds were the best adapted. The eyes were significantly more affected by the environmental effects and therefore could be used to identify animals under heat stress.
The traditional techniques of estrus detection may have some limitations in herds, directly compromising the reproductive efficiency and longevity of animals (Perez Marques et al., 2019). IRT has been applied as a tool to facilitate estrus or ovulation detection. In a study, Vicentini et al. (2020), showed that IRT is a tool to detect temperature variation during the proestrus and estrus phases in heifers, and that the regions around the vulva exhibited the highest temperature. Perez Marques et al. (2019) identified increase of the infrared temperature of 0.5°C and 1.20°C into 48 and 24 hours, respectively, before ovulation in various regions of the body during the estrus in cows, concluding that the IRT can be useful in identifying of pregnancy dairy cows, in estrus, cyclic or non-cyclic. Talukder et al. (2014) also reported an increase of 1.50ºC in the vulva surface temperature of cows 24 hours before the start of ovulation and a regression to normal 48 hours after ovulation, and that the IRT was able to identify 83% of the cows in estrus. According to Ruediger et al. (2018), the ability to detect estrus or ovulation can be due to the increase of tissue vascularization and blood flow of the vulva surface in females in estrus. Therefore, IRT has enormous potential for monitoring animal reproduction, aiming to improve herd fertility rates.
Management techniques prone to influence animal behavior, such as fear and pain, are among many factors that compromise animal welfare and livestock profitability.
Therefore, the ability to measure fear in non-invasive ways is essential to assess animal behavior and welfare, to identify and correct actions that cause discomfort (Cannas et al. 2018). According to Sammer et al. (2019), the application of new tools able to identify management practices that cause fear and pain in cattle is necessary. Stewart et al. (2008) evaluating the ability of IRT to detect stressed cattle after management practices, registered that the eye temperature quickly reduced after handling, and this may be associated to the level of fear or pain of animals, suggesting that the IRT can be used to assess the degree of stress caused by different management practices at commercial livestock farms.
One of those techniques that can cause discomfort and fear in beef cattle is weighing. In most farms, the monitoring of weight gain is done by weighing the animals on scales, which requires restraining, causing discomfort and stress. However, research has evaluated the capacity of the IRT to assist and facilitate the handling of cattle weighing. Stajnko et al. (2008) found positive correlations between infrared body temperatures and live weight in beef cattle, and that IRT can be used to estimate body weight quickly and without the need to contain the animals. According to Sammer et al.
(2019), the application of these modern technologies that aim to adapt management systems is essential to maintain the productivity of the animal industry.
Animal feeding contributes about 70% of production costs, and animals with low feed efficiency can increase these costs. The ability of animals to use energy and convert it into products is called "feed efficiency". According to Leão et al. (2018), animals with high feed efficiency have lower residual food intake (negative intake), while animals with low feed efficiency have higher residual food intake (positive intake). Schaefer et al. (2018) reported that this information is fundamental to increase the productivity and sustainability of livestock production systems. However, Berry et al. (2014) revealed that these measurements have high operational cost in a large population of animals.
Conventional methods, such as calorimetry and feed intake, cost approximately US $300.00/animal (Schaefer et al., 2018). So, researchers have shown that the IRT can be an alternative to assess the association between body surface temperature and physiological processes related to feed efficiency, especially on commercial farms (Montanholi et al., 2008). Leão et al. (2018) identified that the eye infrared temperatures were significantly higher (0.5°C) in calves with high feed efficiency, i.e., lower dry matter intake (-0.14 kg/day), when compared to calves with low feed efficiency, i.e., high dry matter intake (0.13 kg/day), suggesting that the IRT is a tool capable of identifying calves with better feed efficiency. Montanholi et al. (2009) recorded moderate correlations between infrared temperature of eyes, cheeks, paws and residual food intake, dry matter intake and the weight gain in adult beef cattle, indicating that their infrared temperature can be useful to facilitate the assessment of feed efficiency in adult beef cattle. Schaefer et al. (2018) registered an increase of 0.37°C in cheek infrared temperature in dairy cows with positive residual food intake (1.93 kg/day), when compared to the animals with negative residual food intake (-1.76 kg/day). The authors concluded that the IRT is a quick and noninvasive method to measure the metabolic efficiency in dairy cattle due to the positive correlation (0.39) between residual food intake and cheek temperature.

Buffalo
In recent years the IRT has been applied to different goals in buffalo production, such as evaluation of thermal stress, body temperature, thermoregulation, and semen quality, among others. Body infrared temperature can be used as an indicator of thermal stress on a determined environment (Salles et al. 2016). IRT can detect the body temperature without the use of a rectal thermometer (Candido et al., 2020), that the skin surface temperature measured by IRT can be a better indicator of thermal comfort than the respiratory rate. According to , when an animal is under heat stress, the thermoregulation will involve physiological homeostatic mechanisms that will increase heat transfer from the core to the body periphery. This occurs due to the change in blood flow from the core to the skin surface and/or increased respiratory rate, at body periphery vasodilation occurs, in the skin, regulating the release of heat into the environment.  negatively correlated with sperm abnormality (-0.17). Animals with higher scrotal temperature gradient (≥ 6.5°C) had better semen quality than those with an inferior gradient (≤ 4.0°C and 4.1 -6.4°C). According to these results, the greater the temperature gradient, the better the sperm quality, and that IRT can be used as a tool to assess the reproductive performance of buffalo bulls. Ahirwar et al. (2018) showed that the higher the air temperature and humidity index, the higher the superficial testicle IRT of buffalo bulls, and consequently, the higher the abnormal sperm rate, concluding that the scrotal IRT was enough to identify the environmental variables affecting semen quality. According to Chacur (2017), that is due to positive correlation between scrotal temperature and semen quality, satisfactorily indicating the semen quality. Nonetheless, semen quality in buffalo bulls can be associated with the testicle coverage thickness, which can compromise the testicle heat loss. According to Yadav et al. (2019), buffalo bulls with little testicle coverage thickness have a lower percentage of abnormal sperm than buffalo bulls with greater testicle coverage, and this may be due to greater amount of scrotal heat loss and greater thermoregulatory capacity of buffalo bulls with smaller testicle coverage.

Ovine and caprine
The choosing of animals more adapted to climatic change is a decisive factor to obtain good productive and reproductive rates. The maintenance of body temperature reflects the thermoregulation ability of animals. Hansen (2009), reported that during heat stress the animals regulate body temperature, reducing food intake, which decreases metabolic heat production, maintaining ideal body temperature. According to Montanholi et al. (2009), the metabolic heat produced is distributed to the body through the blood, however, when animals are exposed to high ambient temperature, peripheral vasodilation occurs, increasing blood flow to the skin to dissipate internal heat to the environment.  (2015) showed that lambs less efficient in thermoregulation had higher IRT and lower carcass weight. These authors concluded that the lighter carcasses could be associated with reduced food intake, compromising the productivity of animals. Silva et al. (2014), evaluating the adaptation of Parda Alpina and Anglo-Nubiana dairy goats to dry weather, reported that the neck, rump, thigh, and flank IRT presented differences between breeds. The highest infrared temperatures and respiratory rates were recorded in the Parda Alpina breed, therefore, being considered less adapted to dry weather.
In a study about the use of IRT to register a physiological reaction through the change in eye temperature as response to stress and fear during handling, Cannas et al. (2018) suggested that IRT combined with behavioral data can identify the stress and make inference about negative emotions in sheep. IRT allows the monitoring of herd health without direct contact with animals. The use of IR as an image diagnostic method has been tested for some respiratory diseases, such as enzootic sheep nasal adenocarcinoma.
This disease is characterized as a tumor in the upper airways, causing pressure around the nasal bone, leading to deformation of the bone or of the entire skull in more severe cases.
The IRT image of the nostril of a healthy animal had blue and green colors ( Figure 4A), while in sick animals, IRT images showed red and white in the injured region of the nose. This is because in healthy animals, the air that travels through the nostril cools the area, while in sick animals, the air does not penetrate normally, causing the injured area to heat up, displaying color red or white, Figure 4B   variations in udder surface temperature of ewes associated with the inflammatory process caused by mastitis. Martins et al. (2013) reported that IRT is a promising technique to detect subclinical mastitis in ewes. According to these authors, this may be due to, in the acute process, during subclinical mastitis, the affected region produces a higher temperature, while in clinical mastitis, the temperature is lower.
The IRT has been reported as a useful tool for identifying the variation in surface temperature of the vulva in estrus goats. Façanha et al. (2018) identified an increase in temperature in the vulva region by infrared thermography ( Figure 5B and Figure 5C).
According to these authors, the accuracy and agility of IRT, when combined with visual detection of estrus and estrogen hormone levels in Canindé goats, is a faster and more accurate option for estrus detection by breeders. However, more studies are needed.

Swine
The monitoring and controlling of ambient temperature, and the maintaining optimal thermal conditions are the main difficulties for pig production. Some researchers have shown that the IRT can facilitate the measurement of body temperature in swine due to the association between body IRT and rectal temperature. In a recent study, Schmitt and Driscoll (2021) evaluating the IRT as an alternative to measure temperature of piglets after birth, registered a stronger correlation between rectal temperature and ear base IRT.
According to authors, piglets with lower birth weight had less IRT and higher risk of hypothermia, confirming that IRT could be used to investigate the risk of hypothermia in piglets. Justino et al. (2014) evaluated the heat loss and variables related to the thermal comfort of lactating sows submitted to an evaporative cooling system during the summer.
The results indicated that the evaporative cooling system significantly reduced the skin surface temperature in 0.47°C when compared to sows in natural ventilation, and increased heat losses by convection and evaporation, resulting in lower skin surface temperature. In another study, Cook et al. (2015) reported that IRT can be used to detect febrile responses and behavioral changes after vaccination against Parvovirus in weaned piglets. They affirmed that 3 h after getting the vaccine, the animals showed higher body surface temperatures and grouping behavior, when compared to unvaccinated animals ( Figure 6A and Figure 6B). The IRT is a tool for obtaining precise measurement of cardiorespiratory signals in swine (Pereira et al., 2019). Boileau et al. (2019) showed that the dorsal plane is the best anatomical region for thermographic studies in pigs when compared to the eye or ear. The IRT can be used to obtain measures and responses associated with stress situations, and welfare on farm pigs.

Bird
In poultry production, body temperature is obtained by the rectal thermometer.
This method is invasive and causes stress in the animals . So, studies have tested IRT as an alternative to measure the body temperature in birds. Candido et al. (2020) reported a strong correlation between cloacal temperature and body IRT in broiler chickens. The study also recorded 95% accuracy of IRT, suggesting that this technology can be a useful tool to obtain the body temperature in broiler chickens.
In another study, Nascimento et al. (2014) found a high positive correlation between the IRT of poultry facilities and body IRT of broilers chickens. The authors highlighted the importance of the materials of choice, pointing out that they must have low thermal conductivity to reduce heat transfer from the external environment to facilities and to the chickens.
Thermal stress has a negative impact on poultry production. Therefore, in addition to the correct management and suitable poultry facilities, the choice of animals should consider the climatic conditions and the animal's thermoregulation ability (Justino et al., 2014). According to Malcom et al. (2013), body surface temperature can provide information about the degree of thermal stress of animals. In production poultry, Loyau et al. (2016) reported that the body surface temperature of laying hens is an indicator to be used as a selection criterion for climate adaptation in chickens. Furthermore, the authors showed that the IRT is easy to be standardized and automated on farms, providing an accurate temperature reading in large numbers of animals. Alves et al. (2012) reported that laying hens in cold stress expended about four times more energy to keep homeothermy due to the decrease in the ability of birds to consume food. According to Young (1981), the decrease in food intake can be due to the behavioral changes in the animals, such as grouping between laying hens to reduce the loss of body heat. Furthermore, the reduction of egg production may be associated with the deviation of energy to keep the homeothermy, reducing the efficiency of food conversion. Ferreira et al. (2011) evaluating the behavior of body IRT in broilers and diets with different energy levels, showed that broilers fed with diet rich in energy lost less metabolic heat than broilers fed a lower energy diet, and that the IRT was efficient to detect variations in metabolic heat production these animals.
Pododermatitis is a disease of economic importance in poultry which affects the locomotion of the birds, compromising the productivity, carcass quality and egg production. The IRT has been used as a tool to identify pododermatitis in birds. In commercial farms, poultry feet contain soil, feed and other dirt, which compromise the skin emissivity. Moe et al. (2018) evaluating thermal variations by IRT in turkey paws, reported that the maximum foot pad temperature was more accurate in detecting thermal variations and, therefore, could be a good anatomical region used in future thermographic studies of detection of pododermatitis in turkeys. Jacob et al. (2016) revealed that chickens with pododermatitis have a 5.0°C lower surface temperature on the skin of their feet than healthy chickens (Fig. 7.A and Fig. 7

Limitations of the IRT in livestock animals
Even if infrared thermography has some limitations, it can be used in thermographic study of animals to increase the precision of temperature measurement.
The elaboration of specific protocols for each animal species and anatomical region allows to reduce errors and increase the accuracy of IRT in future studies (Moe et al. 2018). Studies have shown that other sources of variation, such as anatomical region, analysis methods, feeding time, camera focus and angle, milking and physical activities of animals before of the measurements should also be considered in thermographic studies (Knížková et al., 2007;Talukder et al., 2014;Moe et al., 2018).
In addition, other factors such as animal handling, non-standardized environment and animal physiology should be taken into account before thermographic analysis (Ricarte et al., 2014). Furthermore, it is necessary to understand the principles related to thermal variations and surface heat exchanges, to know how these thermal distributions can be influenced by the relationship of physiological and metabolic processes with pathologies and adaptive factors.

Perspectives of IRT in livestock animals
Currently, thermal imagers are developed with innovative technology, increasingly affordable acquisition cost and considerable durability (Ricarte et al., 2014).
Besides, the new devices have greater precision, around ±1.0°C , and the thermal images are saved and processed easily, quickly, and can be applied as a routine procedure complementary to clinical examinations in animals (Chacur et al., 2016).
Infrared thermography is a promising method for several goals in livestock production. Due to its non-invasive nature and safe procedures (Castells et al., 2019) IRT provides a way to obtain data in different anatomical regions, without stress (Chacur et al., 2016). The high correlations between normal thermal variations and abnormal thermal variations from inflammatory processes and other clinical data, show that the IRT still has a lot to contribute for livestock production. The technological development of the IRT method should be explored to facilitate the monitoring and controlling of body temperature changes of animals.

CONCLUSIONS
Infrared thermography has been used for several purposes in animal production as it's a non-invasive, accurate and quick tool for detecting changes related to metabolic, physiological, and inflammatory processes in animals. Despite being more used in cattle, IRT can be applied in several animal species and with different purposes, to substitute the conventional methods of diagnosing diseases, inflammatory processes, reproductive stage, semen quality, selection aid, adaptive traits and heat stress. In addition, IRT can quickly identify disease, preventing the spread of contagious maladies to the herd.
This review aims to clarify some difficulties, advantages, and the various possibilities of IRT use in livestock production. However, more studies are needed to improve the thermographic apparatus and software, and to obtain standardized detection models with sensitivity to diagnose physiological and biological changes in the several animal species.

Conflict of interest statement
None