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Table of Contents

    Topic review

    Horses Facial Expressions Machine Recognition

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    Submitted by: Pia Haubro Andersen


    Facial activity can convey valid information about the experience of pain in a horse. The scoring of facial activity is costly and depending on correct observation and interpretation by trained humans. Automatisation would greatly enhance the possibility to detect pain in horses. In humans, emotional states are detected in real time video using automated computer algorithms. However, the application of such methods to horses has proven difficult. Major barriers are the lack of sufficiently large, annotated databases for horses and difficulties in obtaining correct classifications of pain

    1. Background and Aim

    Public concern about equine welfare has increased significantly in recent years, following many reports of wastage and breakdowns in equestrian sport [1][2]. Research across equestrian disciplines has demonstrated that repetitive use injury is the likely precursor to these events [3], so early diagnosis is important. The issue of welfare is pertinent for all stakeholders, from horse owners to horse professionals and veterinarians.
    Despite its importance, there is little consensus among veterinarians and laypersons on the quantitative and qualitative aspects of pain in horses. Clinicians often disagree on the intensity of pain in clinical cases, on whether an affective state of a horse is due to pain. As an example of this lack of consensus, practicing veterinarians can score assumed pain in horses associated with a particular condition on a range from “non-painful” to “very painful” [4][5]. For standard surgeries, such as castration, this variation is unlikely to be attributable solely to variations in the display of pain, but rather to lack of consensus regarding pain recognition. Pain is without a doubt developed as a survival parameter [6], and some veterinarians still believe that “suffering promotes survival”—pain is “good” because it serves a protective function. In a Finnish questionnaire study from 2003, 31% of the veterinarians answered that they somewhat agree that a certain level of pain is useful as it prevents excessive movement after surgery while 86% agreed that animals benefit from pain alleviation [7]. A number of contextual factors can influence both the recognition of pain and pain estimates. No horse studies exist, but in dogs and cattle, veterinarians rating of animal pain is influenced by a number of contextual factors including attitudes to animal pain, gender, age and empathy [7][8][9][10][11] Both pain recognition and pain intensity estimation is reduced in human health care providers after repeated exposure to pain in others [12]. This may be a relevant issue for veterinarians witnessing severe animal pain and suffering, as for example lameness in cows, where veterinarians generally scored pain lower than the farmers [13].
    The lack of consensus is troubling since veterinary decision-making regarding pain recognition is critical for the care of animals in terms of prescribing pain-alleviating treatments and in animal welfare assessments. Freedom from pain, injury and disease is directly specified as one of the five “freedoms” that constitute the minimal standards of animal welfare in European legislation [14]. Veterinarians are subject to a Code of Conduct drawn up by the licensing authority in their country stating that veterinarians should attempt to relieve animal’s pain and suffering as described for example in the European Veterinary Code of Conduct [15]. Animal pain assessment tools that are objective and feasible are therefore wanted for many reasons.
    Some structured tools for pain assessment in horses have been developed in recent decades, mostly for pain diagnosis in specific clinical situations [16][17][18][19]. A pain scale is a formal, structured approach to the assessment of pain. Modern horse pain scales are multi-item scales, based on behavioral and physiological parameters, with the behavioral parameters shown to be more specific to pain than physiological measures [16][17][20][21][22][23]. Physiological parameters, such as heart rate and cortisol blood concentration are correlated significantly with the presence of pain in some studies, but not in others [23]. Physiological parameters may be valid as pain indicators in very controlled settings, but most of them are invasive and require stressful blood sampling or restraint of the animal. Scales comprising the non-invasive observation of body posture, head carriage, location in box and pain behavior, including facial expressions of pain, have been shown to recognize pain in hospital settings [21][24][25], and are therefore interesting targets for automated recognition of pain.
    Human research over the past 20 years has shown consistently that facial expressions can be used as tools for recognizing pain in non-verbal humans [26]. Humans seem to be highly specialized for processing facial cues to recognize emotions, including pain, in con-specifics [27][28]. This has proven useful as a tool in pain assessment in non-verbal humans such as infants [29]. Even facial expressions of durations less than 0.5 s may be interpreted [30]. Social ungulates, such as sheep and horses, also use facial visual cues for recognition of identity and emotional state of conspecifics [31]. How humans interpret animal facial cues and vice versa is less researched but interesting from the perspective of the possible automation of the facial expression. No studies have been performed on horses but have been on other species. In an eye-tracking study, Correia-Caeiro et al. [32] investigated how humans and dogs perceived each other’s facial expressions of emotions. While humans modulated their gaze depending on the area of interest, emotion and species observed, dogs modulated their gaze only on the area of interest. The authors suggested that the differences observed could be driven by automatic brain processes adapted for decoding of faces of conspecifics. For humans to recognize the emotional repertoire in another species, it is therefore necessary to employ learning processes that can overrule these apparently automatic brain processes. While the facial musculature is highly conserved across many non-human species, their meaning, and thus the facial expressions of emotions, including the affective components of pain, may likely be species-specific [32]. In the context of this review, their study underlines the need for objective descriptions of facial activity and interpretations not driven by intuition or expectations.
    The Facial Action Coding System (FACS) [33] is the current gold standard for the objective measurement of facial movements. FACS is a manual, systematic method for identifying and recording facial expressions, based entirely on the movement of underlying facial muscles. FACS exhaustively describes all observable facial behavior in terms of the muscular actions that comprise it, using elements called action units (AUs), and visibility codes are used when parts of the face are not visible [33]. Each AU, designated by an arbitrary numerical code, denotes the movements of an underlying, anatomically defined, facial muscle. The muscular basis of the facial movements described in FACS has been verified by intramuscular stimulation experiments in humans [34]. FACS coders rely on video observation of facial muscle movements and changes in facial morphology to determine which AU(s) occur. The criteria for coding are described in an anatomical, precise language, which increases the agreement between raters. The inter-observer agreement is good to excellent for spontaneously generated facial behavior in 90% of the AUs in humans [35]. Because facial musculature is conserved across mammal species, with some exceptions regarding nose/muzzle and ears, FACS comparisons can be made across species without interpretation biases or other labels.
    FACS has been adapted to several animal species, initially for primates (chimpanzee [36], rhesus macaque [37]; orangutan [38], barbary macaque [37], wild crested macaque [39], Japanese macaque [40], gibbon [41]) and the domestic species such as dogs [42], cats [43] and horses [44]. The development of these modified FACS systems was informed by extensive anatomical work, either through dissection [44][45] and/or intramuscular stimulation of facial muscles in living individuals [34][46].
    The FACS standard has been widely adopted by the human research community owing to the exhaustive nature of FACS descriptions [47][48][49][50] and to the fact that FACS can code all possible movements of the face and not only predetermined expressions. The FACS standard for horses, EquiFACS, was developed in 2015 [44] but has only recently been used for the investigation of affective states such as pain [51] and emotional stress [52] in horses. Manual FACS is not suitable as a clinical tool because it requires frame-by-frame coding of video sequences by a trained and certified FACS reader, and is thus extremely resource-demanding, with coding time requirements at least in the range of 1:100 for the average video, one second of video requiring 100 secs of annotation time.
    For animals, including horses, “grimace scales” have been developed to standardize the evaluation of facial expressions during pain assessment. These scales require fewer inputs than the FACS-based systems and focus on certain described movements and appearance of ears, eye, side of the chin, nostrils and muzzle/nose/snout. The scales are intended for clinical purposes and can be scored directly or via images. The grimace scales thus lack the dynamic component, which may be essential to determine whether a “grimace” is activated or not, which makes the scoring of grimace scales difficult under dynamic conditions, see, for example, [53]. Generally, rater agreement is much influenced by the quality of the description of the feature rated, with a fuzzy or broad description containing subjective elements giving greater variability. Many grimace scales have good performance parameters, and labels are simple, but their feasibility has not yet been validated, which is delaying the full utilization of these scales as pain assessment tools [54]. One drawback of simplifying labels and/or observation time is that rare or dynamic signs of pain may not be included. A certain feature that appears variably during pain experience will not perform well in assessment tools and may therefore be omitted, despite its possible value as a marker of pain and for the internal validity of the scale.
    The development of the many grimace scales clearly shows the need for fast and simple measures of pain. This is also the case for use of facial expressions during complex interactions between animals and humans, such as studies of facial expressions of the horse when moving or being ridden [55][56]. Inspection and annotation of selected images and videos is essential in this type of research, and the selection of horses and footage may be highly prone to different types of bias regarding which footage to select and expectation bias during the subsequent annotation [57].
    An objective tool that could recognize pain or facial expressions reliably, rapidly and inexpensively, would therefore greatly enhance research into pain, validation of scales, quality of surveillance and observation of rapidly changing or subtle facial activities, to mention a few advantages.
    Computer vision (CV) is an approach for the intelligent processing of images and video. The vast majority of modern CV methods use machine learning (ML) to learn their functions and mappings from data examples. CV/ML is part of the wider field of artificial intelligence (AI) and has now advanced to the point where automatic recognition of human facial expressions [58][59][60][61] can be used in behavioral research and in clinical settings [62][63][64]. Fully automated systems have been developed for recognition of the neutral state and six basic human emotions (anger, disgust, fear, joy, sadness and surprise) in video streams of human faces. For example, Littlewort et al. [59] achieved 88% accuracy in the classification of faked or genuine pain and were also able to code videos and images with action unit activations and pain intensities in real-time.
    The major obstruction to the direct application of successful human methods in similar approaches for assessing horse pain is the poor availability of training data. For humans, there are multiple large datasets with image- and video-level expression and action unit annotations [49][65][66], while there are no large publicly available datasets with similar annotations for horses. Good availability of training data would allow modern end-to-end CV/ML techniques, such as those available for humans, to be developed for horses [49][65][66]. The current lack of training data creates a stronger need for hand-engineered algorithms and human labeling and interaction.
    Another important obstacle is the lack of a “gold standard” for pain assessment in animals, which, unlike humans, do not have the ability to self-report. Uncertain or incorrect labeling of pain confuses learning algorithms, ultimately hampering detection of pain. Although modern deep neural network approaches are more robust to labeling noise than conventional learning algorithms [67], algorithms, in general, require vastly more training data if the labeling is inaccurate. The performance of automated systems is therefore heavily influenced by the reliability of the annotations [68].

    2. Biological Challenges and Opportunities in Pain Assessment

    Without entering a discussion of definitions and of how pain is “felt” by animals, the difficulties in the correct classification of pain in horses is a core dilemma, not only for the welfare of horses and the success of veterinary practitioners but also for the development of CV/ML approaches for this task. One concrete example of the latter is that ground truth on pain tends to be reduced to binary labels of whether the horse is in pain or not, even when a range of pain intensities can be obtained. This simplification is necessary to obtain a sufficient number of samples per class, despite data scarcity.
    The nature of pain is biologically quite complex to address but controversy about the conscious experience of the emotional component of pain in animals is fading [54][69][70], with mounting evidence of an emotional component of pain in all vertebrates [71]. The lack of a gold standard for evaluating the affective states of pain in non-verbal mammals has led to the exploration of bodily behavior or physiological markers to convey information about internal states [72].
    The International Association for the Study of Pain IASP defines human pain as “an unpleasant sensory and emotional experience associated with, or resembling that associated with, actual or potential tissue damage” [73]. Because the basic biology and neural apparatus of horses is similar to that of humans, this has led to the use of this definition also for non-human animals such as horses. A review by Sneddon extended this general definition to include that the animal should learn to avoid the noxious stimulus and demonstrate sustained changes in behavior that have a protective function to reduce further injury and pain [69]. While this is perfectly in line with the current understanding of pain-related behavior [74], these criteria are less helpful in the concrete classification of clinical pain. Further, it is generally accepted that no single physiological or biochemical parameter is pathognomonic for pain in horses [24][25], that animals cannot verbalize their pain and that evolutionary heritage may induce prey animals to hide their pain from conspecifics and potential enemies [26][75]. Equids, being prey animals, display pain behaviors that are less obvious to humans [76][77], especially in the presence of unknown or threatening human observers, such as veterinarians. A recent extension to the prey animal narrative is the finding that discomfort behaviors after surgery are expressed less obviously also when a caretaker communicates with the horse, again leading to under-estimation of discomfort [78].
    These circumstances can influence both the pain behaviors and the validity of human classification of pain or no pain and may therefore lead to questions about the validity of footage recorded for subsequent CV analysis. This is particularly important if the classification is intended as a label to guide the training of an ML model.

    3. Requirements on Video Recordings for Use in Computer Vision

    In the following section, we list a number of practical issues we have encountered in our interdisciplinary collaboration. Video recordings of horses in the proximity of, or even communicating with, humans should always be labeled accordingly, if used for CV/ML purposes. Before more details emerge about how the presence of humans influences facial expressions, it seems most advisable to use video segments of pain behavior recorded with minimal external influence. Multicamera settings are ideal, especially if both sides of the face should be coded, for example, in laterality studies, or to avoid invisibility. Some of the most widely used horse pain scales involve social interaction between the observer and the horse, that is, touching, feeding the horse or palpating the sore area [18]. A recent study [79] showed that these types of scales generally perform well, but if the pain is evaluated using one of these scales by direct observation, video recordings for CV/ML purposes should be made immediately before the direct pain scoring. It is also important to test the system in another population of horses, to prevent reliance on spurious correlations. Ideally, each horse should be filmed during different levels of pain, to enable a split between model training and test data according to individual subjects. These preliminary criteria are similar to those recommended for pain scale development in general [54]. Post-recording processing requires blinding and randomization before selecting images or videos for annotation, in order to avoid different types of bias, such as selection bias and expectation bias [57].
    The demand for video or image quality in CV, in terms of the level of resolution and light conditions, is surprisingly modest. According to CV studies [80] and our experience, 224 × 224 pixels and 25 fps are sufficient for processing images and video in modern CV systems (typically artificial neural networks).

    4. Will a Pain Scale Deliver Ground Truth?

    To determine whether a pain scale can deliver ground truth, it is necessary to know the performance parameters of the pain scale used for the actual population tested during the actual conditions. Surprisingly, few pain scales are adequately validated in this regard [54][79] since sensitivity and specificity can only be measured against ground truth. In horses, a number of pain assessment scales based on facial expressions have been presented recently. In 2014, two independent research groups published novel investigations of facial expressions of pain in horses [81][82], showing that horses exhibit a range of facial expressions when experiencing episodes of acute pain. In one of these studies [81], pain was induced in otherwise healthy horses using known pain induction models, whereas the horses in the other study [82] were clinical cases of hospitalized horses with post-operative pain resulting from castration. Both studies identified changes in the same areas of the face, corresponding to moveable facial muscles related to the ears, eyes, nostrils, lips and chin. While the horses in the castration study had undergone anesthesia six hours before the scoring, the horses in the experimental study were unmedicated but trained to stand in front of the camera. Interestingly, the features described still corresponded rather well to the more formal EquiFACS ontology described by [44], with minor differences, for example, whether the horses in the castration study displayed orbital tightening more often than the experimental horses, which could be a sign of tiredness or sickness. The horse grimace scale has since been used successfully for other painful conditions, such as laminitis [83]. The Equine Utrecht University Scale for Facial Assessment of Pain (EQUUS-FAP) was developed using a number of facial activities, including ear and eyelid position, nostril size and muscle tone of the head and the lip in combination with head movement and specific gross pain behaviors [17]. EQUUS-FAP has since been used to assess pain in horses with colic and head pain [84].
    In animals, a correlation between the intensity of facial expression and pain has been reported in mice [85]. Two currently used face-based scales for horses, the Horse Grimace Scale (HGS) [82] and EQUUS-FAP [17][86], use levels of intensity for each individual facial score. For example, the levels in HGS are expressed as “not present, 0 points”, “moderately present, 1 point” or “obviously present 2 points”, where “obviously present” adds double the weight of “moderately present” to the total pain score. In the case of the ears, the different levels represent three different action units, and therefore inferences about correlations between the intensity of an action unit and pain intensity are not justifiable in terms of FACS, but only in terms of grimaces. The Equine Pain Face described by Gleerup et al. [81] does not include the summing of individual facial features, but an observer determines, based on direct observation or from reviewing video recording, whether a pain face is present or not, a process not free of bias. High scores on a pain scale shown to perform well under relevant conditions can be taken to indicate a high likelihood that the horse is in pain. Unfortunately, very few pain scales define cut-off values between “pain” and “no pain”, which is needed for the high usability of a pain scale. For that reason, it is difficult to determine that a horse is not in pain. In some studies, for example [16][19][20], this has led to the inclusion of a subjective assessment of the global pain, which occurs as a category in addition to the otherwise well-defined categories of horse behaviors. For comparison, other pain assessment tools may be added [54]. Subjective assessments, including those provided by expert raters, may be of limited value as ground truth (see e.g., [87]). However, to avoid the logical fallacy of a circular argument, it is of importance to include pain assessments that are not relying on the same categories as investigated in a CV/ML study. If facial action units are to be detected, the pain assessment should then rely on, for example, bodily behaviors.
    Thorough training of the pain rater is important for the reliability of a pain scale. A recent study found that raters of the Horse Grimace Scale showed surprisingly low inter-rater agreement, with a 30-min training session being insufficient for inexperienced raters to obtain satisfactory inter-rater agreement [88]. In a pilot study investigating whether 25 individuals from different backgrounds could assess clinical pain in 18 videos of horses following a 20-min training session on facial expressions of pain, Gleerup et al. [54] found that the participants scored the horses correctly in 61–94% (mean 82%) of the cases. However, the median pairwise Cohen’s Kappa value was 0.48 and the pairwise Spearman correlation of the intensity of the pain face was 0.51, which indicates only modest inter-rater agreement. Movement, stress, coat color and nervous behavior of the horse hampered correct interpretation [89]. Sensitivity and specificity could not be calculated, due to the pilot nature of the study and lack of knowledge of the true pain status of the horses.
    In contrast to experimental individuals, clinical cases are often very diverse in respect to age, gender, breed and coat color, all of which can influence pain assessment [90][91]. They are also diverse in terms of temperament [92], earlier experiences and learnings about pain, hospitals, emotional states, transportation and other pain-influencing factors [93][94]. A clinical approach for convergence towards “ground truth” is to record the presence of the (rather few) behaviors reported to be specifically associated with pain, for example, lameness. However, it is debatable whether the intensity of pain is correlated with the degree of lameness if the pain diminishes during unloading of the limb. Objective measurements of perceived sound horses have revealed that 73% show movement asymmetries which might qualify the horse for a full veterinary lameness examination, if referred [95]. It is therefore important to note that not all movement resembling mild lameness is associated with pain, even when measured objectively. In some rare instances, animal experiments may be considered in order to obtain reliable pain labels in cases where clinical data alone cannot provide the information necessary to inform a network. This carries ethical concerns, strict respect for the animal and ethical control. Many management and treatment procedures are indeed quite painful in humans as in horses, and filming of clinical procedures may yield information about facial expressions, which, however, may be blended with other affects. Fully reversible short-term pain induction treatments in horses include a sole pressure model [96], an inflammatory joint model [79][97][98], a non-invasive ischemic pain model [81] and a capsaicin skin sensitization model [81]. An experimental setup allows recording of proper baseline behaviors, while the short-term pain model predicts the time points for pain and subsequent relief of pain. The equine repertoire of facial activities during pain has been shown to be relatively similar for clinical pain [82] and experimental pain [81]. When using experimental pain for the determination of facial activities, validation of the results in clinical pain patients is important [51]. In summary, pain will remain a subjective experience, and there will probably never be a general “gold standard” or biomarker for pain in horses or other animals for that sake. Computer vision and ML methods, therefore, need to circumvent this.

    5. Analysis of EquiFACS Data

    An alternative to the human interpretation of grimaces for assessing pain is the systematic, objective scoring of the visible movement of individual facial muscles over time. This allows the facial repertoire to be fully described and not limited by the categories of the pain assessment tool at stake. The resulting dataset can then be analyzed by data-driven methods for pain or other interpretation after the coding. This means that FACS is not concerned with any theory and the coder need not be familiar with horses or their behavior, which may be an advantage for the blinding procedures which should always be performed. Learning EquiFACS coding is systematized, and learners have to pass a certification exam [44]. In contrast to this, methodologies for analyzing the final FACS dataset are sparse for horses. For humans, Kunz et al. [66] describe the current approaches for the identification of AUs associated with pain. A common method is to apply two criteria: the AU must comprise more than 5% of total pain AU occurrences for coding at a certain frequency and the AU must occur more frequently during pain than during baseline [99]. This method, which is based on an empirical cut-off value of 5%, seems to work well also in horses [51], as it defines AUs and action descriptors (ADs) (facial movements where the muscular basis either cannot be identified or is the result of a different muscle set, e.g., deep muscles). The final ratings are generally in agreement with those obtained using HGS and the pain face category in the Equine Pain Scale [81][82]. However, the method does not take into consideration the temporal aspects of the onset and offset of the various action units. The method also does not define AUs or ADs that might be rare, but important, for pain detection in the horse. We, therefore, developed graph-based statistical methods that describe the co-occurrence of AUs and methods for detecting AUs that co-occur (conjoined AUs) over varying periods of time [51][52]. A more complex picture emerged when this co-occurrence method was applied. Chewing (AD81) was found to be important, despite low frequency. Eye white increase (AD1) and inner brow raiser (AU101) were selected across all observation time lengths. When we used the co-occurrence graph to determine the conjoined pain AUs, we saw that more AUs of the lower face were identified as indicative of pain, including the chin raiser (AU17), nostril dilator (AD38) and chewing action (AD81) identified previously and also the lip pucker (AU18) and upper lip raiser (AU10). On applying the same statistical methods to sound horses subjected to stressful interventions [52], we observed increased frequencies of eye white increase (AD1), nostril dilator (AD38), upper eyelid raiser (AU5), inner brow raiser (AU101) and tongue show (AD19), along with an increase in “ear flicker” and “blink frequency”. These results show that ML can be successfully applied on FACS data for horses to reveal more distinct interpretations of the affective states of pain and stress. A limitation of these two very small datasets is that there seems to be some overlap between the facial activities of pain and the facial activities of stress, affecting, for example, the specificity of the findings related to the eye and nostril. This is not surprising, since pain is regarded as an internal stressor and can activate the hypothalamo-pituitary-adrenal axis [100], but it may impair the specificity of face-based pain scales, since high levels of stress may be present during pain evaluations. Furthermore, affective states such as fatigue or residual effects from pharmacological sedatives or anesthetics in the clinical setting may affect how the horse displays pain [101].
    Interpretation of the dynamics of facial expressions is an important road forward. Wathan et al. [44] claim that certain facial movements can only be distinguished accurately from sequences. Our FACS-based results seem to corroborate this, an example is the identification of increased frequency of the half blink (AU47) as a new indicator for horses in pain in [51], but further research is needed on interpretation of facial dynamics during mixed affective states. The importance of the loss of temporal information in still images of humans is discussed by Kunz et al. [102], who showed that not all core features of a pain face are present at the same time in all individuals. The frequencies of occurrence of the prototypical pain expressions ranged from 10% to 60%, leading the authors to conclude that the likelihood that all four key facial activities occurred simultaneously might be very low. Similarly, we found that only a very small proportion (6.1%) of frames in the pain videos contained three or more pain AUs [51]. This impedes accurate pain assessment on the basis of randomly selected frames, as the chances of accurately assessing a frame as a horse in pain would be only 6.1%, making this method very insensitive for recognition of pain. Longer observation times are therefore necessary. Automated detection of facial activities may solve some of these issues relating to large differences between the scoring of frames versus direct scoring from video, as already addressed by [53].

    6. Automated Extraction of Facial Features from Images

    Automated pain detection based on EquiFACS in horses requires preliminary efforts to detect and locate a horse face in an image or video clip and to detect individual (EquiFACS) action units. Existing standard methods within CV/ML for object detection can be fine-tuned to recognize specific object classes. In the “Horse Face Finder” [103] we fine-tuned an object detection neural network to detect frames when a horse shows its face to the camera, which further distinguished between different angles of the face (side-view or a 45-degree view relative to the camera), from videos of horses standing in a box. This is an important aid for the otherwise time-consuming selection of sequences from videos that are usable for annotation of equine facial expressions. Importantly, this tool can help reduce selection bias when studying facial expressions in horses using video recordings.
    Importantly, the Horse Face Finder enables facial expression analysis of videos of unrestrained horses in arbitrary positions relative to the camera. As a result, human supervision of the horse before or during filming becomes unnecessary. In fact, human expression datasets such as [49][65][104] that show human faces in full frontal view of the camera are not only difficult to collect but have limited generalization to natural settings where a face is likely to move in and out of the camera view. As a result, face detection and alignment—via facial keypoint detection—are standard preprocessing steps to expression analysis, for example as in [105].

    The entry is from 10.3390/ani11061643


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