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Animals : an open access journal from MDPI2022; 12(18); 2400; doi: 10.3390/ani12182400

Facial Expressions of Horses Using Weighted Multivariate Statistics for Assessment of Subtle Local Pain Induced by Polylactide-Based Polymers Implanted Subcutaneously.

Abstract: Facial-expression-based analysis has been widely applied as a pain coding system in horses. Herein, we aimed to identify pain in horses undergoing subcutaneously polylactide-based polymer implantation. The sham group was submitted only to surgical incision. The horses were filmed before and 24 and 48 h after implantation. Five statistical methods for evaluating their facial expressions (FEs) were tested. Primarily, three levels of scores (0, 1, and 2) were applied to the seven FEs (ear movements, eyebrow tension, orbicularis tension, dilated nostrils, eye opening, muzzle tension, and masticatory muscles tension). Subsequently, the scores of the seven FEs were added (SUM). Afterwards, principal component analysis (PCoA) was performed using the scores of the seven FEs obtained using the first method. Subsequently, weights were created for each FE, based on each variable's contribution variability obtained from the PCoA (SUM.W). Lastly, we applied a general score (GFS) to the animal's face (0 = without pain; 1 = moderate pain; 2 = severe pain). The mechanical nociceptive threshold (MNT) and cutaneous temperature (CT) values were collected at the same moments. The results show no intra- or intergroup differences, when evaluating each FE separately or in the GFS. In the intragroup comparison and 48 h after implantation, the control group showed higher values for SUM, PCoA, and SUM.W, although the horses implanted with polymers displayed more obvious alterations in the CT and MNT. Our findings show that the five statistical strategies used to analyze the faces of the horses were not able to detect low-grade inflammatory pain.
Publication Date: 2022-09-13 PubMed ID: 36139260PubMed Central: PMC9495041DOI: 10.3390/ani12182400Google Scholar: Lookup
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  • Journal Article

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.

The research closely scrutinizes how effectively facial expressions in horses can hint towards subtle pain caused by the subcutaneous placement of polylactide-based polymers. Despite the utilization of five different statistical strategies, the research concedes that none of these techniques proved successful in diagnosing low-grade inflammatory pain in the subjects.

Objective

The research endeavored to identify and evaluate pain in horses after undergoing implantation of polylactide-based polymers, which was tracked via an observational analysis of the horses’ facial expressions. Five different statistical methods were tested in an attempt to accurately assess any subtle pain felt by the horses.

Methodology

  • Horses were reviewed before the procedure and after 24 and 48 hours of having the polymer implants.
  • A series of facial expressions, specifically ear movements, eyebrow tension, orbicularis tension (surrounding the eye), dilated nostrils, eye opening, muzzle tension, and masticatory muscles tension, were allocated a score from 0 to 2.
  • These scores were then added to create a total score(SUM).
  • A principal component analysis (PCoA) was conducted, using the scores from the seven facial expressions.
  • Weighing scales were then set for each facial expression, based on the variability contribution of each variable gleaned via PCoA (SUM.W).
  • Lastly, a general face score (GFS) was calculated, ranging from 0 (denoting no pain) to 2 (severe pain).
  • Cutaneous temperature (CT) and mechanical nociceptive threshold (MNT) metrics were also collected at the same intervals.

Results

  • The results suggested that neither singular facial expression analysis nor the GFS demonstrated any significant intra-group or inter-group differences.
  • A deeper examination revealed that while the control group had higher SUM, PCoA, and SUM.W metrics 48 hours after implantation, the horses with polymer implants revealed more pronounced alterations in CT and MNT readings.

Conclusion

The study concludes that facial expression analysis via the five statistical methods employed could not reliably detect low-grade inflammatory pain in horses post implantation. Therefore, alternatives to these statistical strategies should be explored for improved detection of pain in horses.

Cite This Article

APA
Carvalho JRG, Trindade PHE, Conde G, Antonioli ML, Funnicelli MIG, Dias PP, Canola PA, Chinelatto MA, Ferraz GC. (2022). Facial Expressions of Horses Using Weighted Multivariate Statistics for Assessment of Subtle Local Pain Induced by Polylactide-Based Polymers Implanted Subcutaneously. Animals (Basel), 12(18), 2400. https://doi.org/10.3390/ani12182400

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 12
Issue: 18
PII: 2400

Researcher Affiliations

Carvalho, Júlia R G
  • Department of Animal Morphology and Physiology, School of Agricultural and Veterinarian Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.
Trindade, Pedro H E
  • Department of Veterinary Surgery and Animal Reproduction, School of Veterinary Medicine and Animal Science, São Paulo State University, FMVZ/UNESP, Botucatu 18618-681, SP, Brazil.
Conde, Gabriel
  • Department of Animal Morphology and Physiology, School of Agricultural and Veterinarian Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.
Antonioli, Marina L
  • Department of Veterinary Clinical and Surgery, School of Agricultural and Veterinary Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.
Funnicelli, Michelli I G
  • Department of Technology, School of Agricultural and Veterinary Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.
Dias, Paula P
  • Department of Materials Engineering, São Carlos School of Engineering, University of São Paulo, EESC/USP, São Carlos 13563-120, SP, Brazil.
Canola, Paulo A
  • Department of Veterinary Clinical and Surgery, School of Agricultural and Veterinary Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.
Chinelatto, Marcelo A
  • Department of Materials Engineering, São Carlos School of Engineering, University of São Paulo, EESC/USP, São Carlos 13563-120, SP, Brazil.
Ferraz, Guilherme C
  • Department of Animal Morphology and Physiology, School of Agricultural and Veterinarian Sciences, São Paulo State University, FCAV/UNESP, Jaboticabal 14884-900, SP, Brazil.

Grant Funding

  • 2017/10959-4 / Su00e3o Paulo Research Foundation

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of commercial or financial relationships that could be interpreted as potential conflicts of interest.

References

This article includes 80 references
  1. Webster J. Animal Welfare: Freedoms, Dominions and "A Life Worth Living".. Animals (Basel) 2016 May 24;6(6).
    doi: 10.3390/ani6060035pmc: PMC4929415pubmed: 27231943google scholar: lookup
  2. Price DD. Psychological and neural mechanisms of the affective dimension of pain.. Science 2000 Jun 9;288(5472):1769-72.
    doi: 10.1126/science.288.5472.1769pubmed: 10846154google scholar: lookup
  3. McKune CM, Murrel JC, Nolan AM, White KL, Wright BD. Nociception and pain. .
  4. 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(3):e0263854.
  5. Mullard J, Berger JM, Ellis AD, Dyson S. Development of an ethogram to describe facial expressions in ridden horses (FEReq). J Veter Behav 2017;18:7–12.
  6. Gleerup KCB, Lindegaard C. Recognition and quantification of pain in horses: A tutorial review. Equine Vet Educ 2015;28:47–57.
    doi: 10.1111/eve.12383google scholar: lookup
  7. Trindade PHE, Taffarel MO, Luna SPL. Spontaneous Behaviors of Post-Orchiectomy Pain in Horses Regardless of the Effects of Time of Day, Anesthesia, and Analgesia.. Animals (Basel) 2021 May 31;11(6).
    doi: 10.3390/ani11061629pmc: PMC8230028pubmed: 34072875google scholar: lookup
  8. Silva NEOF, Trindade PHE, Oliveira AR, Taffarel MO, Moreira MAP, Denadai R, Rocha PB, Luna SPL. Validation of the Unesp-Botucatu composite scale to assess acute postoperative abdominal pain in sheep (USAPS).. PLoS One 2020;15(10):e0239622.
  9. Broom DM. Animal welfare: concepts and measurement.. J Anim Sci 1991 Oct;69(10):4167-75.
    doi: 10.2527/1991.69104167xpubmed: 1778832google scholar: lookup
  10. de Grauw JC, van Loon JP. Systematic pain assessment in horses.. Vet J 2016 Mar;209:14-22.
    doi: 10.1016/j.tvjl.2015.07.030pubmed: 26831169google scholar: lookup
  11. Taffarel MO, Luna SP, de Oliveira FA, Cardoso GS, Alonso Jde M, Pantoja JC, Brondani JT, Love E, Taylor P, White K, Murrell JC. Refinement and partial validation of the UNESP-Botucatu multidimensional composite pain scale for assessing postoperative pain in horses.. BMC Vet Res 2015 Apr 1;11:83.
    doi: 10.1186/s12917-015-0395-8pmc: PMC4393617pubmed: 25888751google scholar: lookup
  12. Luna SPL, de Araújo AL, da Nóbrega Neto PI, Brondani JT, de Oliveira FA, Azerêdo LMDS, Telles FG, Trindade PHE. Validation of the UNESP-Botucatu pig composite acute pain scale (UPAPS).. PLoS One 2020;15(6):e0233552.
  13. de Oliveira FA, Luna SP, do Amaral JB, Rodrigues KA, Sant'Anna AC, Daolio M, Brondani JT. Validation of the UNESP-Botucatu unidimensional composite pain scale for assessing postoperative pain in cattle.. BMC Vet Res 2014 Sep 6;10:200.
    doi: 10.1186/s12917-014-0200-0pmc: PMC4172785pubmed: 25192598google scholar: lookup
  14. Mott RO, Hawthorne SJ, McBride SD. Blink rate as a measure of stress and attention in the domestic horse (Equus caballus).. Sci Rep 2020 Dec 8;10(1):21409.
    doi: 10.1038/s41598-020-78386-zpmc: PMC7722727pubmed: 33293559google scholar: lookup
  15. Gigliuto C, De Gregori M, Malafoglia V, Raffaeli W, Compagnone C, Visai L, Petrini P, Avanzini MA, Muscoli C, Viganò J, Calabrese F, Dominioni T, Allegri M, Cobianchi L. Pain assessment in animal models: do we need further studies?. J Pain Res 2014;7:227-36.
    doi: 10.2147/JPR.S59161pmc: PMC4020878pubmed: 24855386google scholar: lookup
  16. Guedes A. Pain Management in Horses.. Vet Clin North Am Equine Pract 2017 Apr;33(1):181-211.
    doi: 10.1016/j.cveq.2016.11.006pubmed: 28325179google scholar: lookup
  17. Ekman P, Friesen WV. Facial Action Coding System: A Technique for the Measurement of Facial Movement. 1st ed. Consulting Psychologists Press; London, UK: 1978.
  18. Jordan A, Hughes J, Pakresi M, Hepburn S, O'Brien JT. The utility of PAINAD in assessing pain in a UK population with severe dementia.. Int J Geriatr Psychiatry 2011 Feb;26(2):118-26.
    doi: 10.1002/gps.2489pubmed: 20652872google scholar: lookup
  19. Chang J, Versloot J, Fashler SR, McCrystal KN, Craig KD. Pain assessment in children: validity of facial expression items in observational pain scales.. Clin J Pain 2015 Mar;31(3):189-97.
    doi: 10.1097/AJP.0000000000000103pubmed: 24810648google scholar: lookup
  20. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, Glick S, Ingrao J, Klassen-Ross T, Lacroix-Fralish ML, Matsumiya L, Sorge RE, Sotocinal SG, Tabaka JM, Wong D, van den Maagdenberg AM, Ferrari MD, Craig KD, Mogil JS. Coding of facial expressions of pain in the laboratory mouse.. Nat Methods 2010 Jun;7(6):447-9.
    doi: 10.1038/nmeth.1455pubmed: 20453868google scholar: lookup
  21. 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(4):e35656.
  22. Matsumiya LC, Sorge RE, Sotocinal SG, Tabaka JM, Wieskopf JS, Zaloum A, King OD, Mogil JS. Using the Mouse Grimace Scale to reevaluate the efficacy of postoperative analgesics in laboratory mice.. J Am Assoc Lab Anim Sci 2012 Jan;51(1):42-9.
    pmc: PMC3276965pubmed: 22330867
  23. Dalla Costa E, Pascuzzo R, Leach MC, Dai F, Lebelt D, Vantini S, Minero M. Can grimace scales estimate the pain status in horses and mice? A statistical approach to identify a classifier.. PLoS One 2018;13(8):e0200339.
  24. Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, Mapplebeck JC, Wei P, Zhan S, Zhang S, McDougall JJ, King OD, Mogil JS. The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions.. Mol Pain 2011 Jul 29;7:55.
    doi: 10.1186/1744-8069-7-55pmc: PMC3163602pubmed: 21801409google scholar: lookup
  25. Liao L, Long H, Zhang L, Chen H, Zhou Y, Ye N, Lai W. Evaluation of pain in rats through facial expression following experimental tooth movement.. Eur J Oral Sci 2014 Apr;122(2):121-4.
    doi: 10.1111/eos.12110pubmed: 24428464google scholar: lookup
  26. Sperry MM, Yu YH, Welch RL, Granquist EJ, Winkelstein BA. Grading facial expression is a sensitive means to detect grimace differences in orofacial pain in a rat model.. Sci Rep 2018 Sep 17;8(1):13894.
    doi: 10.1038/s41598-018-32297-2pmc: PMC6141616pubmed: 30224708google scholar: lookup
  27. 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(9):e44437.
  28. Hedenqvist P, Trbakovic A, Thor A, Ley C, Ekman S, Jensen-Waern M. Carprofen neither reduces postoperative facial expression scores in rabbits treated with buprenorphine nor alters long term bone formation after maxillary sinus grafting.. Res Vet Sci 2016 Aug;107:123-131.
    doi: 10.1016/j.rvsc.2016.05.010pubmed: 27473985google scholar: lookup
  29. Haddad Pinho R, Luna SPL, Esteves Trindade PH, Augusto Justo A, Santilli Cima D, Werneck Fonseca M, Watanabe Minto B, Del Lama Rocha F, Miller A, Flecknell P, Leach MC. Validation of the rabbit pain behaviour scale (RPBS) to assess acute postoperative pain in rabbits (Oryctolagus cuniculus).. PLoS One 2022;17(5):e0268973.
  30. Miller AL, Clarkson JM, Quigley C, Neville V, Krall C, Geijer-Simpson A, Flecknell PA, Leach MC. Evaluating Pain and Analgesia Effectiveness Following Routine Castration in Rabbits Using Behavior and Facial Expressions.. Front Vet Sci 2022;9:782486.
    doi: 10.3389/fvets.2022.782486pmc: PMC8918579pubmed: 35296059google scholar: lookup
  31. Reijgwart ML, Schoemaker NJ, Pascuzzo R, Leach MC, Stodel M, de Nies L, Hendriksen CFM, van der Meer M, Vinke CM, van Zeeland YRA. The composition and initial evaluation of a grimace scale in ferrets after surgical implantation of a telemetry probe.. PLoS One 2017;12(11):e0187986.
  32. 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;205:167–174.
  33. Holden E, Calvo G, Collins M, Bell A, Reid J, Scott EM, Nolan AM. Evaluation of facial expression in acute pain in cats.. J Small Anim Pract 2014 Dec;55(12):615-21.
    doi: 10.1111/jsap.12283pubmed: 25354833google scholar: lookup
  34. Evangelista MC, Watanabe R, Leung VSY, Monteiro BP, O'Toole E, Pang DSJ, Steagall PV. Facial expressions of pain in cats: the development and validation of a Feline Grimace Scale.. Sci Rep 2019 Dec 13;9(1):19128.
    doi: 10.1038/s41598-019-55693-8pmc: PMC6911058pubmed: 31836868google scholar: lookup
  35. Di Giminiani P, Brierley VL, Scollo A, Gottardo F, Malcolm EM, Edwards SA, Leach MC. 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
  36. 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
  37. Navarro E, Mainau E, Manteca X. Development of a Facial Expression Scale Using Farrowing as a Model of Pain in Sows.. Animals (Basel) 2020 Nov 14;10(11).
    doi: 10.3390/ani10112113pmc: PMC7696890pubmed: 33202526google scholar: lookup
  38. Vullo C, Barbieri S, Catone G, Graïc JM, Magaletti M, Di Rosa A, Motta A, Tremolada C, Canali E, Dalla Costa E. Is the Piglet Grimace Scale (PGS) a Useful Welfare Indicator to Assess Pain after Cryptorchidectomy in Growing Pigs?. Animals (Basel) 2020 Mar 2;10(3).
    doi: 10.3390/ani10030412pmc: PMC7143901pubmed: 32131424google scholar: lookup
  39. Gleerup KB, Andersen PH, Munksgaard L, Forkman B. Pain evaluation in dairy cattle. Appl Anim Behav Sci 2015;171:25–32.
  40. Müller BR, Soriano VS, Bellio JCB, Molento CFM. Facial expression of pain in Nellore and crossbred beef cattle. J Vet Behav 2019;34:60–65.
  41. Yamada PH, Codognoto VM, de Ruediger FR, Trindade PHE, da Silva KM, Rizzoto G, Maestá SA, Ferreira JCP, de Soutello RVG, Oba E. Pain assessment based on facial expression of bulls during castration. Appl Anim Behav Sci 2021;236:105258.
  42. McLennan KM, Rebelo CJ, 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.
  43. 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 Nov;132:49-56.
    doi: 10.1016/j.beproc.2016.09.010pubmed: 27693533google scholar: lookup
  44. Häger C, Biernot S, Buettner M, Glage S, Keubler LM, Held N, Bleich EM, Otto K, Müller CW, Decker S, Talbot SR, Bleich A. The Sheep Grimace Scale as an indicator of post-operative distress and pain in laboratory sheep.. PLoS One 2017;12(4):e0175839.
  45. 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(3):e92281.
  46. 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 Dec;206(3):356-64.
    doi: 10.1016/j.tvjl.2015.08.023pubmed: 26526526google scholar: lookup
  47. Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face.. Vet Anaesth Analg 2015 Jan;42(1):103-14.
    doi: 10.1111/vaa.12212pmc: PMC4312484pubmed: 25082060google scholar: lookup
  48. 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 (Basel) 2016 Aug 3;6(8).
    doi: 10.3390/ani6080047pmc: PMC4997272pubmed: 27527224google scholar: lookup
  49. 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.
  50. Lansade L, Nowak R, Lainé AL, Leterrier C, Bonneau C, Parias C, Bertin A. Facial expression and oxytocin as possible markers of positive emotions in horses.. Sci Rep 2018 Oct 2;8(1):14680.
    doi: 10.1038/s41598-018-32993-zpmc: PMC6168541pubmed: 30279565google scholar: lookup
  51. 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(1):e0228130.
  52. Coneglian MM, Borges TD, Weber SH, Bertagnon HG, Michelotto PV. Use of the horse grimace scale to identify and quantify pain due to dental disorders in horses. Appl Anim Behav Sci 2020;225:104970.
  53. Haunhorst FR, Hopster K, Schmicke M, Bienert-Zeit A, Kästner S. Clinical effect of buprenorphine or butorphanol, in combination with detomidine and diazepam, on sedation and postoperative pain after cheek tooth extraction in horses.. Can Vet J 2022 Jan;63(1):39-46.
    pmc: PMC8682929pubmed: 34975166
  54. Kosiara S, Harrison AP. The Effect of Aromatherapy on Equine Facial Expression, Heart Rate, Respiratory Tidal Volume and Spontaneous Muscle Contractures in M. Temporalis and M. Cleidomastoideus. Open J Vet Med 2021;11:87–103.
    doi: 10.4236/ojvm.2021.112005google scholar: lookup
  55. Lundblad J, Rashid M, Rhodin M, Haubro Andersen P. Effect of transportation and social isolation on facial expressions of healthy horses.. PLoS One 2021;16(6):e0241532.
  56. de Oliveira AR, Gozalo-Marcilla M, Ringer SK, Schauvliege S, Fonseca MW, Esteves Trindade PH, Prospero Puoli Filho JN, Luna SPL. Development and validation of the facial scale (FaceSed) to evaluate sedation in horses.. PLoS One 2021;16(6):e0251909.
  57. Ask K, Rhodin M, Tamminen LM, Hernlund E, Haubro Andersen P. Identification of Body Behaviors and Facial Expressions Associated with Induced Orthopedic Pain in Four Equine Pain Scales.. Animals (Basel) 2020 Nov 19;10(11).
    doi: 10.3390/ani10112155pmc: PMC7699379pubmed: 33228117google scholar: lookup
  58. Gregory NS, Harris AL, Robinson CR, Dougherty PM, Fuchs PN, Sluka KA. An overview of animal models of pain: disease models and outcome measures.. J Pain 2013 Nov;14(11):1255-69.
    doi: 10.1016/j.jpain.2013.06.008pmc: PMC3818391pubmed: 24035349google scholar: lookup
  59. Gozalo-Marcilla M, Luna SPL, Gasthuys F, Schauvliege S. Thermal, mechanical and electrical stimuli in antinociceptive studies in standing horses: an update.. Vet Anaesth Analg 2020 Jan;47(1):15-27.
    doi: 10.1016/j.vaa.2019.09.003pubmed: 31813668google scholar: lookup
  60. Casas-Alvarado A, Mota-Rojas D, Hernández-Ávalos I, Mora-Medina P, Olmos-Hernández A, Verduzco-Mendoza A, Reyes-Sotelo B, Martínez-Burnes J. Advances in infrared thermography: Surgical aspects, vascular changes, and pain monitoring in veterinary medicine.. J Therm Biol 2020 Aug;92:102664.
  61. McDonnell S. The Equid Ethogram: A Practical Field Guide to Horse Behavior. 1st ed. Eclipse Press; Amman, Jordan: 2003.
  62. Descovich KA, Wathan J, Leach MC, Buchanan-Smith HM, Flecknell P, Farningham D, Vick SJ. Facial expression: An under-utilised tool for the assessment of welfare in mammals.. ALTEX 2017;34(3):409-429.
    doi: 10.14573/altex.1607161pubmed: 28214916google scholar: lookup
  63. Trindade PHE, Costa FDO, Da Costa MJRP. Expressões faciais em cavalos: Uma abordagem sobre os métodos de avaliação e as limitações de seu uso. Rev Acad Ciên Anim 2018;16:e161109.
  64. 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(11):e0231608.
  65. de Carvalho JRG, Conde G, Antonioli ML, Dias PP, Vasconcelos RO, Taboga SR, Canola PA, Chinelatto MA, Pereira GT, Ferraz GC. Biocompatibility and biodegradation of poly(lactic acid) (PLA) and an immiscible PLA/poly(ε-caprolactone) (PCL) blend compatibilized by poly(ε-caprolactone-b-tetrahydrofuran) implanted in horses. Polym J 2020;52:629–643.
    doi: 10.1038/s41428-020-0308-ygoogle scholar: lookup
  66. Dias PP, Chinelatto MA. Effect of Poly(ε-caprolactone-b-tetrahydrofuran) Triblock Copolymer Concentration on Morphological, Thermal and Mechanical Properties of Immiscible PLA/PCL Blends. J Renew Mater 2019;7:129–138.
    doi: 10.32604/jrm.2019.00037google scholar: lookup
  67. Martin P, Bateson PPG. Measuring Behaviour: An Introductory Guide. 3rd ed. Cambridge University Press; Cambridge, UK: 2007.
    doi: 10.2307/5248google scholar: lookup
  68. Wang FK, Chen JC. Capability index using principal components analysis. Qual Eng 1998;11:21–27.
    doi: 10.1080/08982119808919208google scholar: lookup
  69. Kubrusly LS. Um procedimento para calcular índices a partir de uma base de dados multivariados. Pesqui Oper 2001;21:107–117.
  70. Wathan J, Burrows AM, Waller BM, McComb K. EquiFACS: The Equine Facial Action Coding System.. PLoS One 2015;10(8):e0131738.
  71. Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers.. Biometrics 1977 Jun;33(2):363-74.
    doi: 10.2307/2529786pubmed: 884196google scholar: lookup
  72. Nóbrega FS, Ferreira MP, Facó LL, Selim MB, De Zoppa ALV. Uso da termografia para avaliação da resposta tecidual após implante de polímero a base de poliuretana de mamona em osso III metacarpiano de equinos. Acta Sci Vet 2014;42:1–5.
  73. Carvalho JRG, Conde G, Antonioli ML, Santana CH, Littiere TO, Dias PP, Chinelatto MA, Canola PA, Zara FJ, Ferraz GC. Long-Term Evaluation of Poly(lactic acid) (PLA) Implants in a Horse: An Experimental Pilot Study.. Molecules 2021 Nov 29;26(23).
    doi: 10.3390/molecules26237224pmc: PMC8658935pubmed: 34885807google scholar: lookup
  74. Li RY, Liu ZG, Liu HQ, Chen L, Liu JF, Pan YH. Evaluation of biocompatibility and toxicity of biodegradable poly (DL-lactic acid) films.. Am J Transl Res 2015;7(8):1357-70.
    pmc: PMC4568792pubmed: 26396667
  75. Heber S, Ciotu CI, Hartner G, Gold-Binder M, Ninidze N, Gleiss A, Kress HG, Fischer MJM. TRPV1 antagonist BCTC inhibits pH 6.0-induced pain in human skin.. Pain 2020 Jul;161(7):1532-1541.
  76. Bussières G, Jacques C, Lainay O, Beauchamp G, Leblond A, Cadoré JL, Desmaizières LM, Cuvelliez SG, Troncy E. Development of a composite orthopaedic pain scale in horses.. Res Vet Sci 2008 Oct;85(2):294-306.
    doi: 10.1016/j.rvsc.2007.10.011pubmed: 18061637google scholar: lookup
  77. Hayashi K, Ikemoto T, Ueno T, Arai YP, Shimo K, Nishihara M, Suzuki S, Ushida T. Discordant Relationship Between Evaluation of Facial Expression and Subjective Pain Rating Due to the Low Pain Magnitude.. Basic Clin Neurosci 2018 Jan-Feb;9(1):43-50.
    doi: 10.29252/nirp.bcn.9.1.43pmc: PMC6015640pubmed: 29942439google scholar: lookup
  78. Lindegaard C, Vaabengaard D, Christophersen MT, Ekstøm CT, Fjeldborg J. Evaluation of pain and inflammation associated with hot iron branding and microchip transponder injection in horses.. Am J Vet Res 2009 Jul;70(7):840-7.
    doi: 10.2460/ajvr.70.7.840pubmed: 19566469google scholar: lookup
  79. Erber R, Wulf M, Becker-Birck M, Kaps S, Aurich JE, Möstl E, Aurich C. Physiological and behavioural responses of young horses to hot iron branding and microchip implantation.. Vet J 2012 Feb;191(2):171-5.
    doi: 10.1016/j.tvjl.2011.08.008pubmed: 21917490google scholar: lookup
  80. Hair JJF, Black WC, Babin BJ, Anderson RE. Multivariate Data Analysis. 7th ed. Pearson Education; Upper Saddle River, NJ, USA: 2014.

Citations

This article has been cited 5 times.
  1. Hall C, Kay R. Living the good life? A systematic review of behavioural signs of affective state in the domestic horse (Equus caballus) and factors relating to quality of life. Part 2: Horse-human interactions. Anim Welf 2024;33:e41.
    doi: 10.1017/awf.2024.41pubmed: 39469043google scholar: lookup
  2. de Carvalho JRG, Del Puppo D, Littiere TO, de Sales NAA, Silva ACY, Ribeiro G, de Almeida FN, Alves BG, Gatto IRH, Ramos GV, Ferraz GC. Functional infrared thermography imaging can be used to assess the effectiveness of Maxicam Gel(®) in pre-emptively treating transient synovitis and lameness in horses. Front Vet Sci 2024;11:1399815.
    doi: 10.3389/fvets.2024.1399815pubmed: 38919154google scholar: lookup
  3. Auer U, Kelemen Z, Vogl C, von Ritgen S, Haddad R, Torres Borda L, Gabmaier C, Breteler J, Jenner F. Development, refinement, and validation of an equine musculoskeletal pain scale. Front Pain Res (Lausanne) 2023;4:1292299.
    doi: 10.3389/fpain.2023.1292299pubmed: 38312997google scholar: lookup
  4. 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 Jan 2;14(1):129.
    doi: 10.1038/s41598-023-50383-ypubmed: 38167926google scholar: lookup
  5. da Silva GV, Pivato GM, Peres BG, Luna SPL, Pairis-Garcia MD, Trindade PHE. Simplified assessment of castration-induced pain in pigs using lower complexity algorithms. Sci Rep 2023 Dec 1;13(1):21237.
    doi: 10.1038/s41598-023-48551-1pubmed: 38040949google scholar: lookup