FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Pain / Measurement properties of grimace scales for pain assessment...
Pain2021; 163(6); e697-e714; doi: 10.1097/j.pain.0000000000002474

Measurement properties of grimace scales for pain assessment in nonhuman mammals: a systematic review.

Abstract: Facial expressions of pain have been identified in several animal species. The aim of this systematic review was to provide evidence on the measurement properties of grimace scales for pain assessment. The protocol was registered (SyRF#21-November-2019), and the study is reported according to the PRISMA guidelines. Studies reporting the development, validation, and the assessment of measurement properties of grimace scales were included. Data extraction and assessment were performed by 2 investigators, following the COnsensus-based Standards for the Selection of Health Measurement INstruments guidelines. Six categories of measurement properties were assessed: internal consistency, reliability, measurement error, criterion and construct validity, and responsiveness. Overall strength of evidence (high, moderate, and low) of each instrument was based on methodological quality, number of studies, and studies' findings. Twelve scales for 9 species were included (mice, rats, rabbits, horses, piglets, sheep or lamb, ferrets, cats, and donkeys). Considerable variability regarding their development and measurement properties was observed. The Mouse, Rat, Horse and Feline Grimace Scales exhibited high level of evidence. The Rabbit, Lamb, Piglet and Ferret Grimace Scales and Sheep Pain Facial Expression Scale exhibited moderate level of evidence. The Sheep Grimace Scale, EQUUS-FAP, and EQUUS-Donkey-FAP exhibited low level of evidence for measurement properties. Construct validity was the most reported measurement property. Reliability and other forms of validity have been understudied. This systematic review identified gaps in knowledge on the measurement properties of grimace scales. Further studies should focus on improving psychometric testing, instrument refinement, and the use of grimace scales for pain assessment in nonhuman mammals.
Copyright © 2021 International Association for the Study of Pain.
Get Full Text
Publication Date: 2021-09-09 PubMed ID: 34510132DOI: 10.1097/j.pain.0000000000002474Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Systematic Review
  • Research Support
  • Non-U.S. Gov't

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 study systematically reviews the effectiveness of grimace scales used to evaluate pain in nonhuman mammals. It found that grimace scales are reliable and valid in some species, but more research is needed to improve these tools.

Objective of the Study

  • The researchers aim to evaluate the measurement properties of grimace scales used to assess pain in nonhuman mammals.
  • This systematic review follows the protocol registered under SyRF#21-November-2019, and reported as per PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines.

Methodology

  • The study included scales that reported the development, validation, and assessment of measurement properties of grimace scales in nonhuman mammals.
  • Two investigators were involved in data extraction and assessment, following the guidelines set by the Consensus-based Standards for the Selection of Health Measurement Instruments (COSMIN).
  • Six categories of measurement properties were assessed: internal consistency, reliability, measurement error, criterion and construct validity, and responsiveness.
  • The strength of evidence was classified into high, moderate, and low, based on methodological quality, the number of studies, and findings of these studies.

Study Findings

  • Twelve scales for nine species (mice, rats, rabbits, horses, piglets, lambs, ferrets, cats, and donkeys) were evaluated.
  • There was substantial variability in the development and measurement properties of these scales across species.
  • The Mouse, Rat, Horse, and Feline Grimace Scales showed the highest levels of evidence.
  • The Rabbit, Lamb, Piglet and Ferret Grimace Scales, along with the Sheep Pain Facial Expression Scale, demonstrated a moderate level of evidence.
  • The Sheep Grimace Scale, EQUUS-FAP, and EQUUS-Donkey-FAP showed a low level of evidence.
  • Construct validity was the most reported measurement property.
  • Reliability and other forms of validity were understudied, indicating room for improvement in these areas.

Conclusions and Recommendations

  • The review identified knowledge gaps in the measurement properties of grimace scales.
  • The authors recommend further studies to improve psychometric testing, refine instrument design, and enhance the use of grimace scales for nonhuman mammalian pain assessment.

Cite This Article

APA
Evangelista MC, Monteiro BP, Steagall PV. (2021). Measurement properties of grimace scales for pain assessment in nonhuman mammals: a systematic review. Pain, 163(6), e697-e714. https://doi.org/10.1097/j.pain.0000000000002474

Publication

Pain
ISSN: 1872-6623
NlmUniqueID: 7508686
Country: United States
Language: English
Volume: 163
Issue: 6
Pages: e697-e714

Researcher Affiliations

Evangelista, Marina C
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
Monteiro, Beatriz P
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
Steagall, Paulo V
  • Department of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, Canada.
  • Department of Veterinary Clinical Sciences, Centre for Animal Health and Welfare, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong, S.A.R.

MeSH Terms

  • Animals
  • Cats
  • Facial Expression
  • Ferrets
  • Horses
  • Mice
  • Pain / diagnosis
  • Pain / veterinary
  • Pain Measurement
  • Psychometrics
  • Rabbits
  • Rats
  • Reproducibility of Results
  • Sheep
  • Swine

References

This article includes 105 references
  1. Akintola T, Raver C, Studlack P, Uddin O, Masri R, Keller A. The grimace scale reliably assesses chronic pain in a rodent model of trigeminal neuropathic pain.. Neurobiol Pain 2017;2:13–17.
  2. Anil L, Anil SS, Deen J. Pain detection and amelioration in animals on the farm: issues and options.. J Appl Anim Welf Sci 2005;8:261–78.
  3. Banchi P, Quaranta G, Ricci A, Von Degerfeld MM. Reliability and construct validity of a composite pain scale for rabbit (CANCRS) in a clinical environment.. PLoS One 2020;15:e0221377.
  4. Bateson P. Assessment of pain in animals.. Anim Behav 1991;42:827–39.
  5. Chartier LC, Hebart ML, Howarth GS, Whittaker AL, Mashtoub S. Affective state determination in a mouse model of colitis-associated colorectal cancer.. PLoS One 2020;15:e0228413.
  6. Christov-Moore L, Simpson EA, Coudé G, Grigaityte K, Iacoboni M, Ferrari PF. Empathy: gender effects in brain and behavior.. Neurosci Biobehav Rev 2014;46:604–27.
  7. Cohen S, Beths T. Grimace scores: tools to support the identification of pain in mammals used in research.. Animals 2020;10:1726.
  8. 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.
  9. Dai F, Leach M, Macrae AM, Minero M, Costa ED. Does thirty-minute standardised training improve the inter-observer reliability of the horse grimace scale (HGS)? A case study.. Animals 2020;10:781–87.
  10. 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.
  11. 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:e0200339.
  12. 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;6:47–55.
  13. Descovich KA, Wathan J, Leach MC, Buchanan-smith HM, Flecknell P, Farningham D, Vick S. Facial expression : an under-utilised tool for the assessment of welfare in mammals.. ALTEX 2017;34:409–29.
  14. Deuis JR, Dvorakova LS, Vetter I. Methods used to evaluate pain behaviors in rodents.. Front Mol Neurosci 2017;10:1–17.
  15. van Dierendonck MC, Burden FA, Rickards K, van Loon JPAM. 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;10:354–70.
  16. van Dierendonck MC, van Loon JPAM. 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.
  17. Dobromylskyj P, Flecknell PA, Lascelles BD, Livingston A, Taylor P, Waterman-Pearson A. Pain assessment.. 2000; 53–79.
  18. Ekman P, Friesen W. Facial Action Coding System: A technique for the measurement of facial movement.. 1978.
  19. Evangelista MC, Benito J, Monteiro BP, Watanabe R, Doodnaught GM, Pang DSJ, Steagall PV. Clinical applicability of the Feline Grimace Scale: real-time versus image scoring and the influence of sedation and surgery.. PeerJ 2020;8:e8967.
  20. Evangelista MC, Steagall PV. Agreement and reliability of the Feline Grimace Scale among cat owners, veterinarians, veterinary students and nurses.. Sci Rep 2021;11:5262.
  21. 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;9:19128.
  22. Faller KME, 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.
  23. Di Giminiani P, Brierley VLMH, 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.
  24. Gleerup KB, Andersen PH, Munksgaard L, Forkman B. Pain evaluation in dairy cattle.. Appl Anim Behav Sci 2015;171:25–32.
  25. Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face.. Vet Anaesth Analg 2015;42:103–14.
  26. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, Gold MS, Holdcroft A, Lautenbacher S, Mayer EA, Mogil JS, Murphy AZ, Traub RJ. Studying sex and gender differences in pain and analgesia: a consensus report.. PAIN 2007;132:S26–45.
  27. 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;14:1255–69.
  28. Guesgen MJ, Beausoleil NJ, Leach MC, Minot EO, Stewart M, Stafford KJ. Coding and quantification of a facial expression for pain in lambs.. Behav Process 2016;132:49–56.
  29. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, Schünemann HJ. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.. BMJ 2008;336:924–6.
  30. Hager C, Biernot S, Buettner M, Glage S, Keubler LM, Held N, Bleich EM, Otto K, Muller 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:e0175839.
  31. Hawkins P, Bertelsen T. 3Rs-Related and objective indicators to help assess the culture of care.. Animals 2019;9:969.
  32. 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;55:615–21.
  33. Kaplan RM, Saccuzzo DP. Psychological Testing: Principles, Application and Issues.. 2010.
  34. Keating SCJ, 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.
  35. Klein HJ, Bayne KA. Establishing a culture of care, conscience, and responsibility: addressing the improvement of scientific discovery and animal welfare through science-based performance standards.. ILAR J 2007;48:3–11.
  36. Klune CB, Larkin AE, Leung VSY, Pang DSJ. Comparing the Rat Grimace Scale and a composite behaviour score in rats.. PLoS One 2019;14:e0209467.
  37. 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;7:447–9.
  38. Lascelles BDX, Brown DC, Maixner W, Mogil JS. Spontaneous painful disease in companion animals can facilitate the development of chronic pain therapies for humans.. Osteoarthr Cartil 2017;26:175–83.
  39. 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.
  40. Leung VSY, Benoit-Biancamano MO, Pang DSJ. Performance of behavioral assays: the Rat Grimace Scale, burrowing activity and a composite behavior score to identify visceral pain in an acute and chronic colitis model.. Pain Rep 2019;4:e712.
  41. Leung VSY, Zhang EQ, Pang DSJ. Real-time application of the Rat Grimace Scale as a welfare refinement in laboratory rats.. Sci Rep 2016;6:31667.
  42. 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;122:121–4.
  43. van Loon JPAM, 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.
  44. van Loon JPAM, van Dierendonck MC. Monitoring equine head-related pain with the Equine Utrecht University scale for facial assessment of pain (EQUUS-FAP).. Vet J 2017;220:88–90.
  45. van Loon JPAM, van Dierendonck MC. Pain assessment in horses after orthopaedic surgery and with orthopaedic trauma.. Vet J 2019;246:85–91.
  46. MacRae AM, Joanna Makowska I, 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.
  47. Martinez AM, Kak AC. PCA versus LDA.. IEEE Trans Pattern Anal Mach Intell 2001;23:228–33.
  48. 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;51:42–9.
  49. McDowell I. Measuring Health: A guide to rating scales and questionnaires.. 2006.
  50. McLennan KM, Mahmoud M. Development of an automated pain facial expression detection system for sheep (Ovis aries).. Animals 2019;9:196.
  51. McLennan KM, Miller AL, Dalla Costa E, Stucke D, Corke MJ, Broom DM, Leach MC. 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.
  52. 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.
  53. Merola I, Mills DS. Systematic review of the behavioural assessment of pain in cats.. J Feline Med Surg 2016;18:60–76.
  54. Miller AL, Kitson G, Skalkoyannis B, Leach MC. 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.
  55. Miller AL, Kitson GL, Skalkoyannis B, Flecknell PA, Leach MC. Using the mouse grimace scale and behaviour to assess pain in CBA mice following vasectomy.. Appl Anim Behav Sci 2016;181:160–5.
  56. Miller AL, Leach MC. The effect of handling method on the mouse grimace scale in two strains of laboratory mice.. Lab Anim 2016;50:305–7.
  57. Miller AL, Leach MC. The mouse grimace scale: a clinically useful tool?. PLoS One 2015;10:e0136000.
  58. Miller AL, Leach MC. 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.
  59. Mogil JS. Qualitative sex differences in pain processing: emerging evidence of a biased literature.. Nat Rev Neurosci 2020;21:353–65.
  60. 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.
  61. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.. Plos Med 2009;6:e1000097.
  62. Mokkink LB, Boers M, van der Vleuten CPM, Bouter LM, Alonso J, Patrick DL, de Vet HCW, Terwee CB. COSMIN Risk of Bias tool to assess the quality of studies on reliability or measurement error of outcome measurement instruments: a Delphi study.. BMC Med Res Methodol 2020;20:293.
  63. Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, Bouter LM, De Vet HCW. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes.. J Clin Epidemiol 2010;63:737–45.
  64. Mokkink LB, de Vet HCW, Prinsen CAC, Patrick DL, Alonso J, Bouter LM, Terwee CB. COSMIN risk of bias checklist for systematic reviews of patient-reported outcome measures.. Qual Life Res 2018;27:1171–9.
  65. Monteiro BP, Otis C, del Castillo JRE, Nitulescu R, Brown K, Arendt-Nielsen L, Troncy E. Quantitative sensory testing in feline osteoarthritic pain—a systematic review and meta-analysis.. Osteoarthr Cartil 2020;28:885–96.
  66. Moser HL, Abraham AC, Howell K, Laudier D, Zumstein MA, Galatz LM, Huang AH. Cell lineage tracing and functional assessment of supraspinatus tendon healing in an acute repair murine model.. J Orthop Res 2020;jor:24769.
  67. Mota-Rojas D, Olmos-Hernández A, Verduzco-Mendoza A, Hernández E, Martínez-Burnes J, Whittaker AL. The utility of grimace scales for practical pain assessment in laboratory animals.. Animals 2020;10:1838.
  68. Müller BR, Soriano VS, Bellio JCB, Molento CFM. Facial expression of pain in Nellore and crossbred beef cattle.. J Vet Behav 2019;34:60–5.
  69. Nagakura Y, Miwa M, Yoshida M, Miura R, Tanei S, Tsuji M, Takeda H. Spontaneous pain-associated facial expression and efficacy of clinically used drugs in the reserpine-induced rat model of fibromyalgia.. Eur J Pharmacol 2019;864:172716.
  70. Noor A, Zhao Y, Koubaa A, Wu L, Khan R, Abdalla FYO. Automated sheep facial expression classification using deep transfer learning.. Comput Electron Agric 2020;175:105528.
  71. Oliver V, De Rantere D, Ritchie R, Chisholm J, Hecker KG, Pang DSJ. Psychometric assessment of the rat grimace scale and development of an analgesic intervention score.. PLoS One 2014;9:e97882.
  72. Orth EK, Navas González FJ, Iglesias Pastrana C, Berger JM, Jeune SSle, Davis EW, McLean AK. Development of a donkey grimace scale to recognize pain in donkeys (Equus asinus) post castration.. Animals 2020;10:1411.
  73. Philips BH, Weisshaar CL, Winkelstein BA. Use of the rat grimace scale to evaluate neuropathic pain in a model of cervical radiculopathy.. Comp Med 2017;67:34–42.
  74. Prinsen CAC, Mokkink LB, Bouter LM, Alonso J, Patrick DL, de Vet HCW, Terwee CB. COSMIN guideline for systematic reviews of patient-reported outcome measures.. Qual Life Res 2018;27:1147–57.
  75. De Rantere D, Schuster CJ, Reimer JN, Pang DSJ. The relationship between the Rat Grimace Scale and mechanical hypersensitivity testing in three experimental pain models.. Eur J Pain 2016;20:417–26.
  76. Reed WR, Little JW, Lima CR, Sorge RE, Yarar-Fisher C, Eraslan M, Hurt CP, Ness TJ, Gu JG, Martins DF, Li P. Spinal mobilization prevents NGF-induced trunk mechanical hyperalgesia and attenuates expression of CGRP.. Front Neurosci 2020;14:385.
  77. Reid J, Scott EM, Calvo G, Nolan AM. Definitive Glasgow acute pain scale for cats: validation and intervention level.. Vet Rec 2017;180:449.
  78. 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:e0187986.
  79. Rossi HL, See LP, Foster W, Pitake S, Gibbs J, Schmidt B, Mitchell CH, Abdus-Saboor I. Evoked and spontaneous pain assessment during tooth pulp injury.. Sci Rep 2020;10:1–12.
  80. Samy A, Elmetwally M, El-khodery SA. Antinociceptive effect of intravenous regional analgesia in horses underwent selected short-time distal limb surgeries.. J Equine Vet Sci 2020;91:103113.
  81. Schneider LE, Henley KY, Turner OA, Pat B, Niedzielko TL, Floyd CL. Application of the rat grimace scale as a marker of supraspinal pain sensation after cervical spinal cord injury.. J Neurotrauma 2017;34:2982–93.
  82. Schober P, Boer C, Schwarte LA. Correlation coefficients: appropriate use and interpretation.. Anesth Analg 2018;126:1763–8.
  83. Shansky RM, Woolley CS. Considering sex as a biological variable will be valuable for neuroscience research.. J Neurosci 2016;36:11817–22.
  84. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability.. Psychol Bull 1979;86:420–8.
  85. Silva PGdeB, de Lima Martins JO, de Lima Praxedes Neto RA, Mota Lemos JV, Machado LC, Matos Carlos ACA, Alves APNN, Lima RA. Tumor necrosis factor alpha mediates orofacial discomfort in an occlusal dental interference model in rats: the role of trigeminal ganglion inflammation.. J Oral Pathol Med 2020;49:169–76.
  86. Sneddon LU, Elwood RW, Adamo SA, Leach MC. Defining and assessing animal pain.. Anim Behav 2014;97:201–12.
  87. Sorge RE, Martin LJ, Isbester KA, Sotocinal SG, Rosen S, Tuttle AH, Wieskopf JS, Acland EL, Dokova A, Kadoura B, Leger P, Mapplebeck JCS, McPhail M, Delaney A, Wigerblad G, Schumann AP, Quinn T, Frasnelli J, Svensson CI, Sternberg WF, Mogil JS. Olfactory exposure to males, including men, causes stress and related analgesia in rodents.. Nat Methods 2014;11:629–32.
  88. 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;7:55.
  89. Sperry MM, Yu Y, Kartha S, Ghimire P, Welch RL, Winkelstein BA, Granquist EJ. Intra‐articular etanercept attenuates pain and hypoxia from TMJ loading in the rat.. J Orthop Res 2020;38:1316–26.
  90. 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;8:1–10.
  91. Steagall PV, Monteiro BP. Acute pain in cats: recent advances in clinical assessment.. J Feline Med Surg 2019;21:25–34.
  92. Streiner DL. A checklist for evaluation the usefulness of rating scales.. Can J Psychiatry 1993;38:140–8.
  93. Streiner DL, Norman GR. Heath Measurement Scales: A practical guide to their development and use.. 2008.
  94. Sullivan MJL, Bishop SR, Pivik J. The pain catastrophizing scale: development and validation.. Psychol Assess 1995;7:524–32.
  95. Tanei S, Miwa M, Yoshida M, Miura R, Nagakura Y. The method simulating spontaneous pain in patients with nociplastic pain using rats with fibromyalgia-like condition.. MethodsX 2020;7:100826.
  96. Tuttle AH, Molinaro MJ, Jethwa JF, Sotocinal SG, Prieto JC, Styner MA, Mogil JS, Zylka MJ. A deep neural network to assess spontaneous pain from mouse facial expressions.. Mol Pain 2018;14:1744806918763658.
  97. Viscardi AV, Hunniford M, Lawlis P, Leach MC, 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.
  98. Viscardi AV, Turner PV. Efficacy of buprenorphine for management of surgical castration pain in piglets.. BMC Vet Res 2018;14:1–12.
  99. Viscardi AV, Turner PV. Use of Meloxicam or Ketoprofen for piglet pain control following surgical castration.. Front Vet Sci 2018;5:299.
  100. Vullo C, Barbieri S, Catone G, Graïc JM, Magaletti M, Di Rosa A, Motta A, Tremolada C, Canali E, Costa ED. Is the Piglet Grimace Scale (PGS) a useful welfare indicator to assess pain after cryptorchidectomy in growing pigs?. Animals 2020;10:412–22.
  101. Waller BM, Micheletta J. Facial expression in nonhuman animals.. Emot Rev 2013;5:54–9.
  102. Watanabe R, Doodnaught GM, Evangelista MC, Monteiro BP, Ruel HLM, Steagall PV. Inter-rater reliability of the feline grimace scale in cats undergoing dental extractions.. Front Vet Sci 2020;7:302.
  103. Wheeler CHB, Williams ACC, Morley SJ. Meta-analysis of the psychometric properties of the Pain Catastrophizing Scale and associations with participant characteristics.. PAIN 2019;160:1946–53.
  104. Williams AC. Facial expression of pain: an evolutionary account.. Behav Brain Sci 2002;25:439–88.
  105. Zhang EQ, Leung VSY, Pang DSJ. 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.

Citations

This article has been cited 12 times.
  1. Feighelstein M, Ehrlich Y, Naftaly L, Alpin M, Nadir S, Shimshoni I, Pinho RH, Luna SPL, Zamansky A. Deep learning for video-based automated pain recognition in rabbits.. Sci Rep 2023 Sep 6;13(1):14679.
    doi: 10.1038/s41598-023-41774-2pubmed: 37674052google scholar: lookup
  2. Ferlini Agne G, May BE, Lovett A, Simon O, Steel C, Santos L, Guedes do Carmo L, Barbosa B, Werner LC, Daros RR, Somogyi AA, Sykes B, Franklin S. Horse Grimace Scale Does Not Detect Pain in Horses with Equine Gastric Ulcer Syndrome.. Animals (Basel) 2023 May 12;13(10).
    doi: 10.3390/ani13101623pubmed: 37238054google scholar: lookup
  3. Marini D, Monk JE, Campbell DLM, Lee C, Belson S, Small A. Sex impacts pain behaviour but not emotional reactivity of lambs following ring tail docking.. PeerJ 2023;11:e15092.
    doi: 10.7717/peerj.15092pubmed: 37009150google scholar: lookup
  4. Diwan AD, Melrose J. Intervertebral disc degeneration and how it leads to low back pain.. JOR Spine 2023 Mar;6(1):e1231.
    doi: 10.1002/jsp2.1231pubmed: 36994466google scholar: lookup
  5. Paterson EA, O'Malley CI, Moody C, Vogel S, Authier S, Turner PV. Development and validation of a cynomolgus macaque grimace scale for acute pain assessment.. Sci Rep 2023 Feb 24;13(1):3209.
    doi: 10.1038/s41598-023-30380-xpubmed: 36828891google scholar: lookup
  6. Tomacheuski RM, Oliveira AR, Trindade PHE, Oliveira FA, Candido CP, Teixeira Neto FJ, Steagall PV, Luna SPL. Reliability and Validity of UNESP-Botucatu Cattle Pain Scale and Cow Pain Scale in Bos taurus and Bos indicus Bulls to Assess Postoperative Pain of Surgical Orchiectomy.. Animals (Basel) 2023 Jan 20;13(3).
    doi: 10.3390/ani13030364pubmed: 36766253google scholar: lookup
  7. Pinho RH, Justo AA, Cima DS, Fonseca MW, Minto BW, Rocha FDL, Leach MC, Luna SPL. Effects of Human Observer Presence on Pain Assessment Using Facial Expressions in Rabbits.. J Am Assoc Lab Anim Sci 2023 Jan 1;62(1):81-86.
    doi: 10.30802/AALAS-JAALAS-22-000056pubmed: 36755205google scholar: lookup
  8. Tomacheuski RM, Monteiro BP, Evangelista MC, Luna SPL, Steagall PV. Measurement properties of pain scoring instruments in farm animals: A systematic review using the COSMIN checklist.. PLoS One 2023;18(1):e0280830.
    doi: 10.1371/journal.pone.0280830pubmed: 36662813google scholar: lookup
  9. Tang SN, Bonilla AF, Chahine NO, Colbath AC, Easley JT, Grad S, Haglund L, Le Maitre CL, Leung V, McCoy AM, Purmessur D, Tang SY, Zeiter S, Smith LJ. Controversies in spine research: Organ culture versus in vivo models for studies of the intervertebral disc.. JOR Spine 2022 Dec;5(4):e1235.
    doi: 10.1002/jsp2.1235pubmed: 36601369google scholar: lookup
  10. Aulehner K, Leenaars C, Buchecker V, Stirling H, Schönhoff K, King H, Häger C, Koska I, Jirkof P, Bleich A, Bankstahl M, Potschka H. Grimace scale, burrowing, and nest building for the assessment of post-surgical pain in mice and rats-A systematic review.. Front Vet Sci 2022;9:930005.
    doi: 10.3389/fvets.2022.930005pubmed: 36277074google scholar: lookup
  11. Reedich EJ, Genry LT, Singer MA, Cavarsan CF, Mena Avila E, Boudreau DM, Brennan MC, Garrett AM, Dowaliby L, Detloff MR, Quinlan KA. Enhanced nociceptive behavior and expansion of associated primary afferents in a rabbit model of cerebral palsy.. J Neurosci Res 2022 Oct;100(10):1951-1966.
    doi: 10.1002/jnr.25108pubmed: 35839339google scholar: lookup
  12. Chiang CY, Chen YP, Tzeng HR, Chang MH, Chiou LC, Pei YC. Deep Learning-Based Grimace Scoring Is Comparable to Human Scoring in a Mouse Migraine Model.. J Pers Med 2022 May 24;12(6).
    doi: 10.3390/jpm12060851pubmed: 35743636google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.