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Frontiers in veterinary science2024; 11; 1436795; doi: 10.3389/fvets.2024.1436795

From facial expressions to algorithms: a narrative review of animal pain recognition technologies.

Abstract: Facial expressions are essential for communication and emotional expression across species. Despite the improvements brought by tools like the Horse Grimace Scale (HGS) in pain recognition in horses, their reliance on human identification of characteristic traits presents drawbacks such as subjectivity, training requirements, costs, and potential bias. Despite these challenges, the development of facial expression pain scales for animals has been making strides. To address these limitations, Automated Pain Recognition (APR) powered by Artificial Intelligence (AI) offers a promising advancement. Notably, computer vision and machine learning have revolutionized our approach to identifying and addressing pain in non-verbal patients, including animals, with profound implications for both veterinary medicine and animal welfare. By leveraging the capabilities of AI algorithms, we can construct sophisticated models capable of analyzing diverse data inputs, encompassing not only facial expressions but also body language, vocalizations, and physiological signals, to provide precise and objective evaluations of an animal's pain levels. While the advancement of APR holds great promise for improving animal welfare by enabling better pain management, it also brings forth the need to overcome data limitations, ensure ethical practices, and develop robust ground truth measures. This narrative review aimed to provide a comprehensive overview, tracing the journey from the initial application of facial expression recognition for the development of pain scales in animals to the recent application, evolution, and limitations of APR, thereby contributing to understanding this rapidly evolving field.
Publication Date: 2024-07-17 PubMed ID: 39086767PubMed Central: PMC11288915DOI: 10.3389/fvets.2024.1436795Google Scholar: Lookup
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  • Journal Article
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Overview

  • This review article explores the evolution of technologies used to recognize pain in animals, highlighting the transition from traditional facial expression-based scales to advanced automated pain recognition systems powered by artificial intelligence (AI).
  • It discusses both the benefits and challenges of these emerging AI-driven approaches and underscores their significance for improving animal welfare and veterinary care.

Background on Facial Expression Pain Recognition

  • Facial expressions are a fundamental means of communication and emotional expression not only in humans but across many animal species.
  • Researchers have developed tools like the Horse Grimace Scale (HGS), which rely on humans identifying specific facial features associated with pain in horses.
  • These methods have advanced the ability to detect pain but have inherent limitations including:
    • Subjectivity due to human interpretation, which can vary between observers.
    • Significant training needs for assessors to reliably use these scales.
    • Costs related to time and expertise.
    • Potential biases that may affect accuracy and consistency.
  • Despite these drawbacks, facial expression-based pain scales have been continually refined for different animal species.

Introduction and Potential of Automated Pain Recognition (APR)

  • To overcome the limitations of manual pain recognition, researchers are turning to Automated Pain Recognition (APR) systems powered by Artificial Intelligence (AI).
  • APR employs technologies like computer vision and machine learning to detect and analyze complex pain signals.
  • Advantages include:
    • Objectivity: Algorithms provide consistent and impartial assessments, reducing human bias.
    • Multimodal data integration: APR can analyze not just facial expressions but also body language, vocalizations, and physiological data (e.g., heart rate), giving a more comprehensive pain assessment.
    • Scalability and efficiency: Automated systems can process large volumes of data quickly without fatigue.
  • Application of AI in this context has transformative implications for:
    • Veterinary medicine—enhancing diagnostics and treatment decisions.
    • Animal welfare—improving the recognition and management of pain in diverse animal populations.

Challenges and Limitations of APR

  • While promising, APR faces several key challenges:
    • Data limitations:
      • Requirement for large, high-quality annotated datasets that represent diverse species and pain conditions.
      • Difficulty in obtaining ground truth labels since animal pain cannot be communicated verbally.
    • Ethical considerations:
      • Ensuring that data collection and monitoring respect animal welfare and privacy.
      • Balancing technological intervention without causing additional stress or harm.
    • Technical robustness and generalizability:
      • Models must be validated across various environments, species, and individual differences to be broadly applicable.
      • Potential risk of algorithmic errors or biases if training data is not comprehensive.

Conclusion and Outlook

  • This narrative review traces the journey from the inception of facial expression recognition in animal pain scales to the cutting-edge use of AI in automated pain detection.
  • The integration of AI offers a powerful opportunity to improve the accuracy, speed, and comprehensiveness of pain assessments in animals.
  • Future efforts should focus on addressing data and ethical challenges, developing standardized protocols and ground truth criteria, and fostering interdisciplinary collaboration between veterinarians, computer scientists, and animal welfare experts.
  • Continued progress in this field has the potential to significantly enhance welfare outcomes by ensuring better pain recognition and management in animals who cannot verbally communicate their discomfort.

Cite This Article

APA
Chiavaccini L, Gupta A, Chiavaccini G. (2024). From facial expressions to algorithms: a narrative review of animal pain recognition technologies. Front Vet Sci, 11, 1436795. https://doi.org/10.3389/fvets.2024.1436795

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 11
Pages: 1436795
PII: 1436795

Researcher Affiliations

Chiavaccini, Ludovica
  • Department of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, Gainesville, FL, United States.
Gupta, Anjali
  • Department of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, Gainesville, FL, United States.
Chiavaccini, Guido
  • Independent Researcher, Livorno, Italy.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 117 references
  1. Ferretti V, Papaleo F. Understanding others: emotion recognition in humans and other animals.. Genes Brain Behav (2019) 18:e12544.
    doi: 10.1111/gbb.12544pubmed: 30549185google scholar: lookup
  2. Williams AC. Facial expression of pain: an evolutionary account.. Behav Brain Sci (2002) 25:439–55.
    doi: 10.1017/S0140525X02000080pubmed: 12879700google scholar: lookup
  3. Kappesser J. The facial expression of pain in humans considered from a social perspective.. Philos Trans R Soc Lond B Biol Sci (2019) 374:20190284.
    doi: 10.1098/rstb.2019.0284pmc: PMC6790380pubmed: 31544612google scholar: lookup
  4. Chambers CT, Mogil JS. Ontogeny and phylogeny of facial expression of pain.. Pain (2015) 156:133.
  5. Pessanha F, Ali Salah A, van Loon T, Veltkamp R. Facial image-based automatic assessment of equine pain.. IEEE Trans Affect Comput (2023) 14:2064–76.
  6. Feighelstein M, Henze L, Meller S, Shimshoni I, Hermoni B, Berko M. Explainable automated pain recognition in cats.. Sci Rep (2023) 13:8973.
    doi: 10.1038/s41598-023-35846-6pmc: PMC10238514pubmed: 37268666google scholar: lookup
  7. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S. Coding of facial expressions of pain in the laboratory mouse.. Nat Methods (2010) 7:447–9.
    doi: 10.1038/nmeth.1455pubmed: 20453868google scholar: lookup
  8. Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS. The rat grimace scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions.. Mol Pain (2011) 7:55.
    doi: 10.1186/1744-8069-7-55pmc: PMC3163602pubmed: 21801409google scholar: lookup
  9. Walter S, Gruss S, Frisch S, Liter J, Jerg-Bretzke L, Zujalovic B. “what about automated pain recognition for routine clinical use?” a survey of physicians and nursing staff on expectations, requirements, and acceptance.. Front Med (2020) 7:566278.
    doi: 10.3389/fmed.2020.566278pmc: PMC7779395pubmed: 33409286google scholar: lookup
  10. Lencioni GC, de Sousa RV, de Souza Sardinha EJ, Corrêa RR, Zanella AJ. Pain assessment in horses using automatic facial expression recognition through deep learning-based modeling.. PLoS ONE (2021) 16:e0258672.
  11. Werner P, Al-Hamadi A, Limbrecht-Ecklundt K, Walter S, Gruss S, Traue HC. Automatic pain assessment with facial activity descriptors.. IEEE Transact Affect Comp (2016) 8:286–99.
  12. Olugbade TA, Bianchi-Berthouze N, Marquardt N, Williams AC. Pain level recognition using kinematics and muscle activity for physical rehabilitation in chronic pain.. In: 2015 International Conference on Affective Computing and Intelligent Interaction (ACII). Xi'an: IEEE; (2015).
  13. Thiam P, Kessler V, Amirian M, Bellmann P, Layher G, Zhang Y. Multi-modal pain intensity recognition based on the senseemotion database.. IEEE Transact Affect Comp (2019) 12:743–60.
  14. Mogil JS, Pang DSJ, Silva Dutra GG, Chambers CT. The development and use of facial grimace scales for pain measurement in animals.. Neurosci Biobehav Rev (2020) 116:480–93.
  15. Oliver V, De Rantere D, Ritchie R, Chisholm J, Hecker KG, Pang DS. Psychometric assessment of the rat grimace scale and development of an analgesic intervention score.. PLoS ONE (2014) 9:e97882.
  16. Matsumiya LC, Sorge RE, Sotocinal SG, Tabaka JM, Wieskopf JS, Zaloum A. Using the Mouse Grimace Scale to reevaluate the efficacy of postoperative analgesics in laboratory mice. J Am Assoc Lab Anim Sci (2012) 51:42–9.
    pmc: PMC3276965pubmed: 22330867
  17. Leach MC, Klaus K, Miller AL, Scotto di Perrotolo M, Sotocinal SG, Flecknell PA. the assessment of post-vasectomy pain in mice using behaviour and the Mouse Grimace Scale. PLoS ONE (2012) 7:e35656.
  18. Faller KM, McAndrew DJ, Schneider JE, Lygate CA. Refinement of analgesia following thoracotomy and experimental myocardial infarction using the Mouse Grimace Scale. Exp Physiol (2015) 100:164–72.
  19. Keating SC, Thomas AA, Flecknell PA, Leach MC. Evaluation of emla cream for preventing pain during tattooing of rabbits: changes in physiological, behavioural and facial expression responses. PLoS ONE (2012) 7:e44437.
  20. Holden E, Calvo G, Collins M, Bell A, Reid J, Scott E. Evaluation of facial expression in acute pain in cats. J Small Anim Pract (2014) 55:615–21.
    doi: 10.1111/jsap.12283pubmed: 25354833google scholar: lookup
  21. Evangelista MC, Watanabe R, Leung VSY, Monteiro BP, O'Toole E, Pang DSJ. Facial expressions of pain in cats: the development and validation of a Feline Grimace Scale. Sci Rep (2019) 9:19128.
    doi: 10.1038/s41598-019-55693-8pmc: PMC6911058pubmed: 31836868google scholar: lookup
  22. Dalla Costa E, Minero M, Lebelt D, Stucke D, Canali E, Leach MC. Development of the Horse Grimace Scale (Hgs) as a pain assessment tool in horses undergoing routine castration. PLoS ONE (2014) 9:e92281.
  23. Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face. Vet Anaesth Analg (2015) 42:103–14.
    doi: 10.1111/vaa.12212pmc: PMC4312484pubmed: 25082060google scholar: lookup
  24. Yamada PH, Codognoto VM, de Ruediger FR, Trindade PHE, da Silva KM, Rizzoto G. Pain assessment based on facial expression of bulls during castration. Appl Anim Behav Sci (2021) 236:105258.
  25. Di Giminiani P, Brierley VL, Scollo A, Gottardo F, Malcolm EM, Edwards SA. The assessment of facial expressions in piglets undergoing tail docking and castration: toward the development of the Piglet Grimace Scale. Front Vet Sci (2016) 3:100.
    doi: 10.3389/fvets.2016.00100pmc: PMC5107875pubmed: 27896270google scholar: lookup
  26. Viscardi AV, Hunniford M, Lawlis P, Leach M, Turner PV. Development of a Piglet Grimace Scale to evaluate piglet pain using facial expressions following castration and tail docking: a pilot study. Front Vet Sci (2017) 4:51.
    doi: 10.3389/fvets.2017.00051pmc: PMC5394162pubmed: 28459052google scholar: lookup
  27. Häger C, Biernot S, Buettner M, Glage S, Keubler LM, Held N. The Sheep Grimace Scale as an indicator of post-operative distress and pain in laboratory sheep. PLoS ONE (2017) 12:e0175839.
  28. Guesgen MJ, Beausoleil NJ, Leach M, Minot EO, Stewart M, Stafford KJ. Coding and quantification of a facial expression for pain in lambs. Behav Processes (2016) 132:49–56.
    doi: 10.1016/j.beproc.2016.09.010pubmed: 27693533google scholar: lookup
  29. Reijgwart ML, Schoemaker NJ, Pascuzzo R, Leach MC, Stodel M, de Nies L. The composition and initial evaluation of a Grimace Scale in ferrets after surgical implantation of a telemetry probe. PLoS ONE (2017) 12:e0187986.
  30. MacRae AM, Makowska IJ, Fraser D. Initial evaluation of facial expressions and behaviours of harbour seal pups (Phoca Vitulina) in response to tagging and microchipping. Appl Anim Behav Sci (2018) 205:167–74.
  31. Orth EK, Navas Gonzalez FJ, Iglesias Pastrana C, Berger JM, Jeune SSL, Davis EW. Development of a Donkey Grimace Scale to recognize pain in donkeys (Equus Asinus) post castration. Animals (2020) 10:1411.
    doi: 10.3390/ani10081411pmc: PMC7459673pubmed: 32823676google scholar: lookup
  32. van Dierendonck MC, Burden FA, Rickards K, van Loon J. Monitoring acute pain in donkeys with the Equine Utrecht University Scale for Donkeys Composite Pain Assessment (EQUUS-Donkey-Compass) and the Equine Utrecht University Scale for Donkey Facial Assessment of Pain (EQUUS-Donkey-Fap). Animals (2020) 10:354.
    doi: 10.3390/ani10020354pmc: PMC7070438pubmed: 32098391google scholar: lookup
  33. Dalla Costa E, Dai F, Lecchi C, Ambrogi F, Lebelt D, Stucke D. Towards an improved pain assessment in castrated horses using facial expressions (Hgs) and circulating mirnas. Vet Rec (2021) 188:e82.
    doi: 10.1002/vetr.82pubmed: 33960478google scholar: lookup
  34. Viscardi AV, Turner PV. Use of meloxicam or ketoprofen for piglet pain control following surgical castration. Front Vet Sci (2018) 5:299.
    doi: 10.3389/fvets.2018.00299pmc: PMC6275193pubmed: 30534552google scholar: lookup
  35. Viscardi AV, Turner PV. Efficacy of buprenorphine for management of surgical castration pain in piglets. BMC Vet Res (2018) 14:1–12.
    doi: 10.1186/s12917-018-1643-5pmc: PMC6199726pubmed: 30352586google scholar: lookup
  36. van Loon JP, Van Dierendonck MC. Monitoring acute equine visceral pain with the Equine Utrecht University Scale for Composite Pain Assessment (EQUUS-Compass) and the Equine Utrecht University Scale for Facial Assessment Of Pain (EQUUS-Fap): a scale-construction study. Vet J (2015) 206:356–64.
    doi: 10.1016/j.tvjl.2015.08.023pubmed: 26526526google scholar: lookup
  37. VanDierendonck MC, van Loon JP. Monitoring acute equine visceral pain with the Equine Utrecht University Scale for Composite Pain Assessment (EQUUS-Compass) and the Equine Utrecht University Scale for Facial Assessment Of Pain (EQUUS-Fap): a validation study. Vet J (2016) 216:175–7.
    doi: 10.1016/j.tvjl.2016.08.004pubmed: 27687948google scholar: lookup
  38. Dalla Costa E, Bracci D, Dai F, Lebelt D, Minero M. Do different emotional states affect the horse Grimace Scale Score? A pilot study. J Eq Vet Sci (2017) 54:114–7.
  39. McLennan KM, Rebelo CJB, Corke MJ, Holmes MA, Leach MC, Constantino-Casas F. Development of a facial expression scale using footrot and mastitis as models of pain in sheep. Appl Anim Behav Sci (2016) 176:19–26.
  40. de Oliveira FA, Luna SP, do Amaral JB, Rodrigues KA, Sant'Anna AC, Daolio M. Validation of the UNESP-Botucatu Unidimensional Composite Pain Scale for assessing postoperative pain in cattle. BMC Vet Res (2014) 10:200.
    doi: 10.1186/s12917-014-0200-0pmc: PMC4172785pubmed: 25192598google scholar: lookup
  41. Dalla Costa E, Stucke D, Dai F, Minero M, Leach MC, Lebelt D. Using the Horse Grimace Scale (Hgs) to assess pain associated with acute laminitis in horses (Equus caballus). Animals (2016) 6:47.
    doi: 10.3390/ani6080047pmc: PMC4997272pubmed: 27527224google scholar: lookup
  42. Miller A, Leach M. Using the Mouse Grimace Scale to assess pain associated with routine ear notching and the effect of analgesia in laboratory mice. Lab Anim (2015) 49:117–20.
    doi: 10.1177/0023677214559084pubmed: 25378137google scholar: lookup
  43. McLennan KM, Miller AL, Dalla Costa E, Stucke D, Corke MJ, Broom DM. Conceptual and methodological issues relating to pain assessment in mammals: the development and utilisation of Pain Facial Expression Scales. Appl Anim Behav Sci (2019) 217:1–15.
  44. Trindade PHE, Hartmann E, Keeling LJ, Andersen PH, Ferraz GC, Paranhos da Costa MJR. Effect of work on body language of ranch horses in Brazil. PLoS ONE (2020) 15:e0228130.
  45. Miller AL, Golledge HD, Leach MC. The influence of isoflurane anaesthesia on the Rat Grimace Scale. PLoS ONE (2016) 11:e0166652.
  46. Miller A, Kitson G, Skalkoyannis B, Leach M. The effect of isoflurane anaesthesia and buprenorphine on the Mouse Grimace Scale and Behaviour in Cba and Dba/2 Mice. Appl Anim Behav Sci (2015) 172:58–62.
  47. Reed RA, Krikorian AM, Reynolds RM, Holmes BT, Branning MM, Lemons MB. Post-anesthetic Cps and Equus-Fap scores in surgical and non-surgical equine patients: an observational study. Front Pain Res (2023) 4:1217034.
    doi: 10.3389/fpain.2023.1217034pmc: PMC10369185pubmed: 37502312google scholar: lookup
  48. Gkikas S, Tsiknakis M. Automatic assessment of pain based on deep learning methods: a systematic review. Comput Methods Progr Biomed (2023) 231:107365.
    doi: 10.1016/j.cmpb.2023.107365pubmed: 36764062google scholar: lookup
  49. Andersen PH, Broomé S, Rashid M, Lundblad J, Ask K, Li Z. Towards machine recognition of facial expressions of pain in horses. Animals (2021) 11:1643.
    doi: 10.3390/ani11061643pmc: PMC8229776pubmed: 34206077google scholar: lookup
  50. Waller BM, Bard KA, Vick S-J, Smith Pasqualini MC. Perceived differences between chimpanzee (Pan Troglodytes) and human (Homo Sapiens) facial expressions are related to emotional interpretation. J Comp Psychol (2007) 121:398.
    doi: 10.1037/0735-7036.121.4.398pubmed: 18085923google scholar: lookup
  51. Lou ME, Porter ST, Massey JS, Ventura B, Deen J, Li Y. The application of 3d landmark-based geometric morphometrics towards refinement of the Piglet Grimace Scale. Animals (2022) 12:1944.
    doi: 10.3390/ani12151944pmc: PMC9367447pubmed: 35953933google scholar: lookup
  52. Koo TK, Li MY. A Guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med (2016) 15:155–63.
    doi: 10.1016/j.jcm.2016.02.012pmc: PMC4913118pubmed: 27330520google scholar: lookup
  53. McLennan K, Mahmoud M. Development of an automated pain facial expression detection system for sheep (Ovis Aries). Animals (2019) 9:196.
    doi: 10.3390/ani9040196pmc: PMC6523241pubmed: 31027279google scholar: lookup
  54. Ekman P, Friesen WV. Manual for the Facial Action Code. Palo Alto, CA: Consulting Psychologists Press; (1978).
  55. Caeiro CC, Waller BM, Zimmermann E, Burrows AM, Davila-Ross M. Orangfacs: a muscle-based facial movement coding system for orangutans ( spp). Int J Primatol (2013) 34:115–29.
    doi: 10.1007/s10764-012-9652-xgoogle scholar: lookup
  56. Parr LA, Waller BM, Vick SJ, Bard KA. Classifying chimpanzee facial expressions using muscle action. Emotion (2007) 7:172–81.
    doi: 10.1037/1528-3542.7.1.172pmc: PMC2826116pubmed: 17352572google scholar: lookup
  57. Correia-Caeiro C, Holmes K, Miyabe-Nishiwaki T. Extending the maqfacs to measure facial movement in Japanese Macaques (Macaca Fuscata) reveals a wide repertoire potential. PLoS ONE (2021) 16:e0245117.
  58. Clark PR, Waller BM, Burrows AM, Julle-Danière E, Agil M, Engelhardt A. Morphological variants of silent bared-teeth displays have different social interaction outcomes in crested macaques (Macaca nigra). Am J Phys Anthropol (2020) 173:411–22.
    doi: 10.1002/ajpa.24129pubmed: 32820559google scholar: lookup
  59. Waller BM, Lembeck M, Kuchenbuch P, Burrows AM, Liebal K. Gibbonfacs: a muscle-based facial movement coding system for hylobatids. Int J Primatol (2012) 33:809–21.
    doi: 10.1007/s10764-012-9611-6google scholar: lookup
  60. Correia-Caeiro C, Burrows A, Wilson DA, Abdelrahman A, Miyabe-Nishiwaki T. Callifacs: The common marmoset facial action coding system. PLoS ONE (2022) 17:e0266442.
  61. Wathan J, Burrows AM, Waller BM, McComb K. Equifacs: the equine facial action coding system. PLoS ONE (2015) 10:e0131738.
  62. Rashid M, Silventoinen A, Gleerup KB, Andersen PH. Equine facial action coding system for determination of pain-related facial responses in videos of horses. PLoS ONE (2020) 15:e0231608.
  63. Waller BM, Peirce K, Caeiro CC, Scheider L, Burrows AM, McCune S. Paedomorphic facial expressions give dogs a selective advantage. PLoS ONE (2013) 8:e82686.
  64. Caeiro CC, Burrows AM, Waller BM. Development and application of catfacs: are human cat adopters influenced by cat facial expressions?. Appl Anim Behav Sci (2017) 189:66–78.
  65. Waller BM, Julle-Daniere E, Micheletta J. Measuring the evolution of facial ‘expression' using multi-species facs. Neurosci Biobehav Rev (2020) 113:1–11.
  66. Mota-Rojas D, Marcet-Rius M, Ogi A, Hernández-Ávalos I, Mariti C, Martínez-Burnes J. Current advances in assessment of dog's emotions, facial expressions, and their use for clinical recognition of pain.. Animals (2021) 11:3334.
    doi: 10.3390/ani11113334pmc: PMC8614696pubmed: 34828066google scholar: lookup
  67. Bennett V, Gourkow N, Mills DS. Facial correlates of emotional behaviour in the domestic cat. Behav Processes (2017) 141:342–50.
    doi: 10.1016/j.beproc.2017.03.011pubmed: 28341145google scholar: lookup
  68. Vojtkovská V, Voslárová E, Večerek V. Methods of assessment of the welfare of shelter cats: a review.. Animals (2020) 10:1–34.
    doi: 10.3390/ani10091527pmc: PMC7552334pubmed: 32872242google scholar: lookup
  69. Finka LR, Luna SP, Brondani JT, Tzimiropoulos Y, McDonagh J, Farnworth MJ. Geometric morphometrics for the study of facial expressions in non-human animals, using the domestic cat as an exemplar.. Sci Rep (2019) 9:9883.
    doi: 10.1038/s41598-019-46330-5pmc: PMC6614427pubmed: 31285531google scholar: lookup
  70. Mullard J, Berger JM, Ellis AD, Dyson S. Development of an ethogram to describe facial expressions in ridden horses (Fereq).. J Vet Behav (2017) 18:7–12.
  71. Dyson S, Berger JM, Ellis AD, Mullard J. Can the presence of musculoskeletal pain be determined from the facial expressions of ridden horses (Fereq)?. J Vet Behav (2017) 19:78–89.
  72. Dyson S, Berger J, Ellis AD, Mullard J. Development of an ethogram for a pain scoring system in ridden horses and its application to determine the presence of musculoskeletal pain.. J Vet Behav (2018) 23:47–57.
  73. Dyson S, Pollard D. Application of the ridden horse pain ethogram to 150 horses with musculoskeletal pain before and after diagnostic anaesthesia.. Animals (2023) 13:1940.
    doi: 10.3390/ani13121940pmc: PMC10295347pubmed: 37370450google scholar: lookup
  74. Dyson S, Pollard D. Application of the ridden horse pain ethogram to horses competing in British eventing 90, 100 and novice one-day events and comparison with performance.. Animals (2022) 12:590.
    doi: 10.3390/ani12050590pmc: PMC8909886pubmed: 35268159google scholar: lookup
  75. Dyson S, Pollard D. Application of the ridden horse pain ethogram to elite dressage horses competing in world cup grand prix competitions.. Animals (2021) 11:1187.
    doi: 10.3390/ani11051187pmc: PMC8143096pubmed: 33919208google scholar: lookup
  76. Ask K, Rhodin M, Rashid-Engström M, Hernlund E, Andersen PH. Changes in the equine facial repertoire during different orthopedic pain intensities.. Sci Rep (2024) 14:129.
    doi: 10.1038/s41598-023-50383-ypmc: PMC10762010pubmed: 38167926google scholar: lookup
  77. Bussières G, Jacques C, Lainay O, Beauchamp G, Leblond A, Cadoré JL. Development of a composite orthopaedic pain scale in horses.. Res Vet Sci (2008) 85:294–306.
    doi: 10.1016/j.rvsc.2007.10.011pubmed: 18061637google scholar: lookup
  78. Christov-Moore L, Simpson EA, Coudé G, Grigaityte K, Iacoboni M, Ferrari PF. Empathy: gender effects in brain and behavior.. Neurosci Biobehav Rev (2014) 46 (Pt 4):604–27.
  79. Zhang EQ, Leung VS, Pang DS. Influence of rater training on inter-and intrarater reliability when using the Rat Grimace Scale.. J Am Assoc Lab Anim Sci (2019) 58:178–83.
  80. Schanz L, Krueger K, Hintze S. Sex and age don't matter, but breed type does-factors influencing eye wrinkle expression in horses.. Front Vet Sci (2019) 6:154.
    doi: 10.3389/fvets.2019.00154pmc: PMC6549476pubmed: 31192235google scholar: lookup
  81. de Oliveira AR, Gozalo-Marcilla M, Ringer SK, Schauvliege S, Fonseca MW, Trindade PHE. Development, validation, and reliability of a sedation scale in horses (Equised).. Front Vet Sci (2021) 8:611729.
    doi: 10.3389/fvets.2021.611729pmc: PMC7921322pubmed: 33665216google scholar: lookup
  82. Kelemen Z, Grimm H, Long M, Auer U, Jenner F. Recumbency as an equine welfare indicator in geriatric horses and horses with chronic orthopaedic disease.. Animals (2021) 11:3189.
    doi: 10.3390/ani11113189pmc: PMC8614510pubmed: 34827921google scholar: lookup
  83. Maisonpierre IN, Sutton MA, Harris P, Menzies-Gow N, Weller R, Pfau T. Accelerometer activity tracking in horses and the effect of pasture management on time budget.. Equine Vet J (2019) 51:840–5.
    doi: 10.1111/evj.13130pubmed: 31009100google scholar: lookup
  84. Podturkin AA, Krebs BL, Watters JV, A. Quantitative approach for using anticipatory behavior as a graded welfare assessment.. J Appl Anim Welf Sci (2023) 26:463–77.
    doi: 10.1080/10888705.2021.2012783pubmed: 35000521google scholar: lookup
  85. Clegg IL, Rödel HG, Delfour F. Bottlenose dolphins engaging in more social affiliative behaviour judge ambiguous cues more optimistically.. Behav Brain Res (2017) 322(Pt A):115–22.
    doi: 10.1016/j.bbr.2017.01.026pubmed: 28110003google scholar: lookup
  86. Foris B, Thompson AJ, von Keyserlingk MAG, Melzer N, Weary DM. Automatic detection of feeding- and drinking-related agonistic behavior and dominance in dairy cows.. J Dairy Sci (2019) 102:9176–86.
    doi: 10.3168/jds.2019-16697pubmed: 31400897google scholar: lookup
  87. Fontaine D, Vielzeuf V, Genestier P, Limeux P, Santucci-Sivilotto S, Mory E. Artificial intelligence to evaluate postoperative pain based on facial expression recognition.. Eur J Pain (2022) 26:1282–91.
    doi: 10.1002/ejp.1948pubmed: 35352426google scholar: lookup
  88. Werner P, Lopez-Martinez D, Walter S, Al-Hamadi A, Gruss S, Picard RW. Automatic recognition methods supporting pain assessment: a survey.. IEEE Transact Affect Comp (2022) 13:530–52.
  89. Dedek C, Azadgoleh MA, Prescott SA. Reproducible and fully automated testing of nocifensive behavior in mice.. Cell Rep Methods (2023) 3:100650.
  90. Broomé S, Feighelstein M, Zamansky A, Carreira Lencioni G, Haubro Andersen P, Pessanha F. Going deeper than tracking: a survey of computer-vision based recognition of animal pain and emotions.. Int J Comput Vis (2023) 131:572–90.
  91. Quinn PC, Palmer V, Slater AM. Identification of gender in domestic-cat faces with and without training: perceptual learning of a natural categorization task.. Perception (1999) 28:749–63.
    doi: 10.1068/p2884pubmed: 10664769google scholar: lookup
  92. Pompermayer E, Hoey S, Ryan J, David F, Johnson JP. Straight Egyptian Arabian skull morphology presents unique surgical challenges compared to the thoroughbred: a computed tomography morphometric anatomical study.. Am J Vet Res (2023) 84:191.
    doi: 10.2460/ajvr.22.11.0191pubmed: 36972699google scholar: lookup
  93. Southerden P, Haydock RM, Barnes DM. Three dimensional osteometric analysis of mandibular symmetry and morphological consistency in cats.. Front Vet Sci (2018) 5:157.
    doi: 10.3389/fvets.2018.00157pmc: PMC6052099pubmed: 30050911google scholar: lookup
  94. Tuttle AH, Molinaro MJ, Jethwa JF, Sotocinal SG, Prieto JC, Styner MA. A deep neural network to assess spontaneous pain from mouse facial expressions.. Mol Pain (2018) 14:1744806918763658.
    doi: 10.1177/1744806918763658pmc: PMC5858615pubmed: 29546805google scholar: lookup
  95. Andresen N, Wöllhaf M, Hohlbaum K, Lewejohann L, Hellwich O, Thöne-Reineke C. Towards a fully automated surveillance of well-being status in laboratory mice using deep learning: starting with facial expression analysis.. PLoS ONE (2020) 15:e0228059.
  96. Broomé S, Ask K, Rashid-Engström M, Haubro Andersen P, Kjellström H. Sharing pain: using pain domain transfer for video recognition of low grade orthopedic pain in horses.. PLoS ONE (2022) 17:e0263854.
  97. Noor A, Zhao Y, Koubaa A, Wu L, Khan R, Abdalla FYO. Automated sheep facial expression classification using deep transfer learning.. Comp Electron Agric (2020) 175:105528.
  98. Broomé S, Gleerup KB, Andersen PH, Kjellstrom H. Dynamics are important for the recognition of equine pain in video.. IEEE/CVF Conference on Computer Vision and Pattern Recognition (2019).
  99. Hummel H, Pessanha F, Salah AA, van Loon JP, Veltkamp R. Automatic pain detection on horse and donkey faces.. 15th IEEE International Conference on Automatic Face and Gesture Recognition. Buenos Aires (2020).
  100. Feighelstein M, Shimshoni I, Finka LR, Luna SPL, Mills DS, Zamansky A. Automated recognition of pain in cats.. Sci Rep (2022) 12:9575.
    doi: 10.1038/s41598-022-13348-1pmc: PMC9187730pubmed: 35688852google scholar: lookup
  101. Martvel G, Lazebnik T, Feighelstein M, Henze L, Meller S, Shimshoni I. Automated pain recognition in cats using facial landmarks: dynamics matter.. Sci Rep (2023).
  102. Feighelstein M, Ehrlich Y, Naftaly L, Alpin M, Nadir S, Shimshoni I. Deep learning for video-based automated pain recognition in rabbits.. Sci Rep (2023) 13:14679.
    doi: 10.1038/s41598-023-41774-2pmc: PMC10482887pubmed: 37674052google scholar: lookup
  103. Lu Y, Mahmoud M, Robinson P. Estimating sheep pain level using facial action unit detection.. 2017 . Washington, DC: IEEE (2017).
  104. Mahmoud M, Lu Y, Hou X, McLennan K, Robinson P. Estimation of pain in sheep using computer vision.. In:Moore RJ, editor. Handbook of Pain and Palliative Care: Biopsychosocial and Environmental Approaches for the Life Course. Cham: Springer International Publishing; (2018). p. 145–57.
  105. Pessanha F, McLennan K, Mahmoud MM. Towards automatic monitoring of disease progression in sheep: a hierarchical model for sheep facial expressions analysis from video.. 2020 15th IEEE International Conference on Automatic Face and Gesture Recognition (FG 2020). Buenos Aires (2002). p. 387–93.
  106. Steagall PV, Monteiro BP, Marangoni S, Moussa M, Sautié M. Fully automated deep learning models with smartphone applicability for prediction of pain using the Feline Grimace Scale.. Sci Rep (2023) 13:21584.
    doi: 10.1038/s41598-023-49031-2pmc: PMC10703818pubmed: 38062194google scholar: lookup
  107. Rashid M, Broomé S, Ask K, Hernlund E, Andersen PH, Kjellström H. Equine pain behavior classification via self-supervised disentangled pose representation.. (2021).
  108. Reulke R, Rueß D, Deckers N, Barnewitz D, Wieckert A, Kienapfel K. Analysis of motion patterns for pain estimation of horses.. 15th IEEE International Conference on Advanced Video and Signal Based Surveillance (AVSS). Auckland: (2018).
  109. Zhu H, Salgirli Y, Can P, Atilgan D, Salah AA. Video-based estimation of pain indicators in dogs.. 2023 11th International Conference on Affective Computing and Intelligent Interaction (ACII). IEEE: (2023).
  110. Mischkowski D, Palacios-Barrios EE, Banker L, Dildine TC, Atlas LY. Pain or nociception? Subjective experience mediates the effects of acute noxious heat on autonomic responses.. Pain (2018) 159:699–711.
  111. Minh D, Wang HX, Li YF, Nguyen TN. Explainable artificial intelligence: a comprehensive review.. Artif Intell Rev (2022) 55:3503–68.
  112. Rashid M, Gu X, Lee YJ. Interspecies knowledge transfer for facial keypoint detection.. IEEE Conference on Computer Vision and Pattern Recognition (CVPR). Honolulu, HI (2017).
  113. Blumrosen G, Hawellek D, Pesaran B. Towards automated recognition of facial expressions in animal models.. IEEE International Conference on Computer Vision Workshops. Washington, DC (2017).
  114. Martvel G, Shimshoni I, Zamansky A. Automated detection of cat facial landmarks.. Int J Comput Vis (2024).
  115. Hassan T, Seus D, Wollenberg J, Weitz K, Kunz M, Lautenbacher S. Automatic detection of pain from facial expressions: a survey.. IEEE Trans Pattern Anal Mach Intell (2021) 43:1815–31.
    doi: 10.1109/TPAMI.2019.2958341pubmed: 31825861google scholar: lookup
  116. McLennan S, Fiske A, Tigard D, Müller R, Haddadin S, Buyx A. Embedded ethics: a proposal for integrating ethics into the development of medical AI. BMC Med Ethics (2022) 23:6.
    doi: 10.1186/s12910-022-00746-3pmc: PMC8793193pubmed: 35081955google scholar: lookup
  117. Norori N, Hu Q, Aellen FM, Faraci FD, Tzovara A. Addressing bias in big data and AI for health care: a call for open science. Patterns (2021) 2:100347.

Citations

This article has been cited 6 times.
  1. Chen Y, Hou R, Chen Z, Lu J, Chen S, Xiong S, Feng J, Robbins TW, Yan H, Xiao X. Cracking the Valence Code: Patterned Facial Kinematics and Neural Signatures of Emotional Expressions in Mice.. Adv Sci (Weinh) 2025 Nov;12(42):e17156.
    doi: 10.1002/advs.202417156pubmed: 40832811google scholar: lookup
  2. Martvel G, Zamansky A, Pedretti G, Canori C, Shimshoni I, Bremhorst A. Dog facial landmarks detection and its applications for facial analysis.. Sci Rep 2025 Jul 1;15(1):21886.
    doi: 10.1038/s41598-025-07040-3pubmed: 40595051google scholar: lookup
  3. Wang H, Shi Z, Hu R, Wang X, Chen J, Che H. Real-time fear emotion recognition in mice based on multimodal data fusion.. Sci Rep 2025 Apr 6;15(1):11797.
    doi: 10.1038/s41598-025-95483-zpubmed: 40189678google scholar: lookup
  4. Bhave A, Kieson E, Hafner A, Gloor PA. Identifying Novel Emotions and Wellbeing of Horses from Videos Through Unsupervised Learning.. Sensors (Basel) 2025 Jan 31;25(3).
    doi: 10.3390/s25030859pubmed: 39943498google scholar: lookup
  5. Parker RL. Comparative analysis of chronic neuropathic pain and pain assessment in companion animals and humans.. Front Vet Sci 2024;11:1520043.
    doi: 10.3389/fvets.2024.1520043pubmed: 39720411google scholar: lookup
  6. Chiavaccini L, Gupta A, Anclade N, Chiavaccini G, De Gennaro C, Johnson AN, Portela DA, Romano M, Vettorato E, Luethy D. Automated acute pain prediction in domestic goats using deep learning-based models on video-recordings.. Sci Rep 2024 Nov 7;14(1):27104.
    doi: 10.1038/s41598-024-78494-0pubmed: 39511381google scholar: lookup