Can grimace scales estimate the pain status in horses and mice? A statistical approach to identify a classifier.
Abstract: Pain recognition is fundamental for safeguarding animal welfare. Facial expressions have been investigated in several species and grimace scales have been developed as pain assessment tool in many species including horses (HGS) and mice (MGS). This study is intended to progress the validation of grimace scales, by proposing a statistical approach to identify a classifier that can estimate the pain status of the animal based on Facial Action Units (FAUs) included in HGS and MGS. To achieve this aim, through a validity study, the relation between FAUs included in HGS and MGS and the real pain condition was investigated. A specific statistical approach (Cumulative Link Mixed Model, Inter-rater reliability, Multiple Correspondence Analysis, Linear Discriminant Analysis and Support Vector Machines) was applied to two datasets. Our results confirm the reliability of both scales and show that individual FAU scores of HGS and MGS are related to the pain state of the animal. Finally, we identified the optimal weights of the FAU scores that can be used to best classify animals in pain with an accuracy greater than 70%. For the first time, this study describes a statistical approach to develop a classifier, based on HGS and MGS, for estimating the pain status of animals. The classifier proposed is the starting point to develop a computer-based image analysis for the automatic recognition of pain in horses and mice.
Publication Date: 2018-08-01 PubMed ID: 30067759PubMed Central: PMC6070187DOI: 10.1371/journal.pone.0200339Google 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.
- Journal Article
- 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.
This research study aims to advance the validation of grimace scales, commonly used for pain assessment in animals like horses and mice, and uses statistical methods to identify a classifier that predicts an animal’s pain status based on its facial expressions. The study’s findings confirm the grimace scale’s reliability and propose a classifier with over 70% accuracy for recognizing pain in horses and mice.
Research Overview
- The research aims to contribute to the validation of grimace scales, which are scales that use facial expressions to assess pain in animals, particularly horses and mice.
- The researchers apply several advanced statistical methods to develop a classifier—a rule or algorithm that helps identify the pain state of an animal based on specific facial movements.
Methods and Approach
- The researchers studied the relationship between Facial Action Units (FAUs), which are distinct facial movements coded in the grimace scales, and actual pain conditions in the animals.
- They applied complex statistical methods–Cumulative Link Mixed Model, Inter-rater reliability, Multiple Correspondence Analysis, Linear Discriminant Analysis, and Support Vector Machines–to two distinct datasets for their analysis.
Results
- The results validate the reliability of both the horse and mouse grimace scales, confirming that individual scores on each FAU correlate with an animal’s pain state.
- The researchers then identified optimal weights for each FAU score, enabling them to classify animals as in pain with an accuracy rate above 70%.
Implications and Future Work
- As a significant development in pain recognition in animals, this research proposes the first statistically sound approach for developing a classifier using horser and mouse grimace scales.
- This classifier serves as a foundation for future work on developing a computer-based image analysis system for automatically recognizing pain in horses and mice, which could significantly enhance animal welfare through better pain management.
Cite This Article
APA
Dalla Costa E, Pascuzzo R, Leach MC, Dai F, Lebelt D, Vantini S, Minero M.
(2018).
Can grimace scales estimate the pain status in horses and mice? A statistical approach to identify a classifier.
PLoS One, 13(8), e0200339.
https://doi.org/10.1371/journal.pone.0200339 Publication
Researcher Affiliations
- Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Milan, Italy.
- MOX Laboratory for Modelling and Scientific Computing, Department of Mathematics, Politecnico di Milano, Milan, Italy.
- Newcastle University, School of Natural and Environmental Sciences, Newcastle upon Tyne, United Kingdom.
- Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Milan, Italy.
- Equine Research & Consulting, Inca, Spain.
- MOX Laboratory for Modelling and Scientific Computing, Department of Mathematics, Politecnico di Milano, Milan, Italy.
- Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, Milan, Italy.
MeSH Terms
- Anesthesia, General
- Anesthetics, Local / administration & dosage
- Animals
- Bupivacaine / administration & dosage
- Discriminant Analysis
- Ear / physiology
- Facial Expression
- Horses
- Male
- Mice
- Nose / physiology
- Pain / pathology
- Pain Measurement / methods
- Support Vector Machine
- Vasectomy
Grant Funding
- Wellcome Trust
- G1100563/1 / National Centre for the Replacement, Refinement and Reduction of Animals in Research
- Biotechnology and Biological Sciences Research Council
Conflict of Interest Statement
Dirk Lebelt is not employed by a commercial company. \"Equine Research & Consulting\" is the name under which he works as an independent researcher and science consultant. He did not receive any funding other the ones declared in the original Funding Statement nor did he act as a funder for this study. \"Equine Research & Consulting\" is a commercial affiliation, that does not alter our adherence to PLOS ONE policies on sharing data and materials.
References
This article includes 41 references
- de Grauw JC, van Loon JPAM. Systematic pain assessment in horses. Veterinary Journal 209: 14–22.
- Ison SH, Clutton RE, Di Giminiani P, Rutherford KMD. A Review of Pain Assessment in Pigs. Frontiers in Veterinary Science 3: 108.
- Weary DM, Niel L, Flower FC, Fraser D. Identifying and preventing pain in animals. Applied Animal Behaviour Science 100: 64–76.
- Bartlett MS, Littlewort GC, Frank MG, Lee K. Automatic decoding of facial movements reveals deceptive pain expressions. Current Biology 24: 738–743.
- Desrosiers A, Harrison D, Letham A. Use of facial expressions for pain assessment in infants during acute painful procedures. Pediatric Pain Letter 17: 1–8.
- Grunau R, Craig K. Pain expression in neonates: facial action and cry. Pain 28: 395–410.
- Heiderich TM, Leslie ATFS, Guinsburg R. Neonatal procedural pain can be assessed by computer software that has good sensitivity and specificity to detect facial movements. Acta Paediatrica 104: e63–e69.
- Lu G, Yang C, Chen M, Li X. Sparse Representation Based Facial Expression Classification for Pain Assessment in Neonates. 12th International Conference on Natural Computation, Fuzzy Systems and Knowledge Discovery pp. 1615–1619.
- Ashraf AB, Lucey S, Cohn JF, Chen T, Ambadar Z, Prkachin KM. The Painful Face—Pain Expression Recognition Using Active Appearance Models. Image and vision computing 27: 1788–1796.
- Schmidt KL, Cohn JF. Human facial expressions as adaptations: Evolutionary questions in facial expression research. American Journal of Physical Anthropology 116: 3–24.
- Lucey P, Cohn JF, Prkachin KM, Solomon PE, Chew S, Matthews I. Painful monitoring: Automatic pain monitoring using the UNBC-McMaster shoulder pain expression archive database. Image and Vision Computing 30: 197–205.
- Lucey P, Cohn JF, Prkachin KM, Solomon PE, Matthews I. Painful data: The UNBC-McMaster shoulder pain expression archive database Face and Gesture 2011. IEEE pp. 57–64.
- Lu G, Li X, Li H. Facial expression recognition for neonatal pain assessment. International Conference on Neural Networks and Signal Processing IEEE.
- Pantic M, Rothkrantz LJM. Machine understanding of facial expression of pain. Behavioral and Brain Sciences 25: 469–470.
- 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 12: e0187986.
- Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S. Coding of facial expressions of pain in the laboratory mouse. Nature methods 7: 447–449.
- Miller AL, Leach MC. The mouse grimace scale: A clinically useful tool?. PloS one 10: 1–10.
- 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 7: e35656.
- 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 9.
- 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 6.
- Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face. Veterinary Anaesthesia and Analgesia 42: 103–114.
- Defensor EB, Corley MJ, Blanchard RJ, Blanchard DC. Facial expressions of mice in aggressive and fearful contexts. Physiology and Behavior 107: 680–685.
- Faller KME, McAndrew DJ, Schneider JE, Lygate CA. Refinement of analgesia following thoracotomy and experimental myocardial infarction using the Mouse Grimace Scale. Experimental physiology 100: 164–172.
- Dalla Costa E, Bracci D, Dai F, Lebelt D, Minero M. Do Different Emotional States Affect the Horse Grimace Scale Score? A Pilot Study. Journal of Equine Veterinary Science 54: 114–117.
- Lecchi C, Dalla Costa E, Lebelt D, Ferrante V, Canali E, Ceciliani F. Circulating miR-23b-3p, miR-145-5p and miR-200b-3p are potential biomarkers to monitor acute pain associated with laminitis in horses. Animal 12: 366–375.
- Agresti A. Analysis of Ordinal Categorical Data. Second Edi Hoboken, NJ, USA: John Wiley & Sons, Inc.
- Christensen RHB. Analysis of ordinal data with cumulative link models—estimation with the ordinal package. R-package .
- McGraw KO, Wong SP. Forming inferences about some intraclass correlation coefficients. Psychological methods 1: 30.
- Cicchetti DV. Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychological Assessment 6: 284–2.
- Gamer M, Lemon J, Singh IFP. Various Coefficients of Interrater Reliability and Agreement. R package .
- Greenacre M, Blasius J. Multiple Correspondence Analysis and Related Methods. London: Chapman & Hall/CRC.
- Greenacre M. Correspondence analysis in practice. Second edi Academic Press, editor London: Chapman & Hall/CRC.
- Husson F, Josse J, Le S, Mazet J. FactoMineR: Multivariate Exploratory Data Analysis and Data Mining. R package .
- Johnson RA, Wichern DW. Applied multivariate statistical analysis. Sixth Edit Upper Saddle River, New Jersey: Pearson Education, Inc.
- Cristianini N, Shawe-Taylor J. An introduction to Support Vector Machine (and other kernel-based learning methods). Cambridge University Press, Cambridge, Massachusetts, USA.
- Venables WN, Ripley BD. Modern Applied Statistics with S. Fourth Edi Springer, New York.
- Karatzoglou A, Smola A, Hornik K, Zeileis A. An S4 Package for Kernel Methods in R. Journal of Statistical Software 11: 1–20.
- Malviya S, Voepel-Lewis T, Burke C, Merkel S, Tait AR. The revised FLACC observational pain tool: Improved reliability and validity for pain assessment in children with cognitive impairment. Paediatric Anaesthesia 16: 258–265.
- Sutton GA, Dahan R, Turner D, Paltiel O. A behaviour-based pain scale for horses with acute colic: scale construction. Veterinary journal 196: 394–401.
- Chatellier G, Zapletal E, Lemaitre D, Menard J, Degoulet P. The number needed to treat: a clinically useful nomogram in its proper context. BMJ 312.
- European Horse Network. Key Figures. 1–4 p..
Citations
This article has been cited 30 times.- Mota-Rojas D, Whittaker AL, Lanzoni L, Bienboire-Frosini C, Domínguez-Oliva A, Chay-Canul A, Fischer V, Hernández-Avalos I, Bragaglio A, Nannoni E, Olmos-Hernández A, Fernandes Bettencourt A, Mora-Medina P, Martínez-Burnes J, Casas-Alvarado A, Grandin T. Clinical interpretation of body language and behavioral modifications to recognize pain in domestic mammals. Front Vet Sci 2025;12:1679966.
- Musial F, Weiss T. What if Horses Were Humans? Comparing Rein Tension and Bit Pressures to Human Pressure Pain Thresholds. Animals (Basel) 2025 Oct 15;15(20).
- Sluka KA, Sowers LP, Fairbanks CA, Lascelles BDX. Moving beyond measures of pain intensity in preclinical models. Pain 2025 Nov 1;166(11S):S52-S54.
- MacKechnie-Guire R, Clayton H, Williams J, Marlin D, Fisher M, Fisher D, Walker V, Murray R. Measuring Noseband Tightness on the Lateral Aspect of the Horse's Face. Animals (Basel) 2025 Feb 13;15(4).
- O'Connell E, Dyson S, McLean A, McGreevy P. No More Evasion: Redefining Conflict Behaviour in Human-Horse Interactions. Animals (Basel) 2025 Jan 31;15(3).
- 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.
- Nakashima SF, Ukezono M, Takano Y. Painful Experiences in Social Contexts Facilitate Sensitivity to Emotional Signals of Pain from Conspecifics in Laboratory Rats. Animals (Basel) 2024 Apr 24;14(9).
- Dai F, Dalla Costa E, Minero M, Briant C. Does housing system affect horse welfare? The AWIN welfare assessment protocol applied to horses kept in an outdoor group-housing system: The 'parcours'. Anim Welf 2023;32:e22.
- Onuma K, Watanabe M, Sasaki N. The grimace scale: a useful tool for assessing pain in laboratory animals. Exp Anim 2024 Jul 9;73(3):234-245.
- Ferguson LT, Rashied AA, Liang Z, Yumoto T, Anyalebechi JC, Swift DA, Hernandes MS, Krafty RT, Coopersmith CM, Lee VK. A Novel Scoring System for Humane Endpoints in Mice with Cecal Ligation and Puncture-Induced Sepsis. Comp Med 2023 Dec 1;73(6):446-460.
- Comin M, Atallah E, Chincarini M, Mazzola SM, Canali E, Minero M, Cozzi B, Rossi E, Vignola G, Dalla Costa E. Events with Different Emotional Valence Affect the Eye's Lacrimal Caruncle Temperature Changes in Sheep. Animals (Basel) 2023 Dec 22;14(1).
- 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).
- Alini M, Diwan AD, Erwin WM, Little CB, Melrose J. An update on animal models of intervertebral disc degeneration and low back pain: Exploring the potential of artificial intelligence to improve research analysis and development of prospective therapeutics. JOR Spine 2023 Mar;6(1):e1230.
- Domínguez-Oliva A, Mota-Rojas D, Hernández-Avalos I, Mora-Medina P, Olmos-Hernández A, Verduzco-Mendoza A, Casas-Alvarado A, Whittaker AL. The neurobiology of pain and facial movements in rodents: Clinical applications and current research. Front Vet Sci 2022;9:1016720.
- Carvalho JRG, Trindade PHE, Conde G, Antonioli ML, Funnicelli MIG, Dias PP, Canola PA, Chinelatto MA, Ferraz GC. Facial Expressions of Horses Using Weighted Multivariate Statistics for Assessment of Subtle Local Pain Induced by Polylactide-Based Polymers Implanted Subcutaneously. Animals (Basel) 2022 Sep 13;12(18).
- Ernst L, Bruch S, Kopaczka M, Merhof D, Bleich A, Tolba RH, Talbot SR. A model-specific simplification of the Mouse Grimace Scale based on the pain response of intraperitoneal CCl(4) injections. Sci Rep 2022 Jun 28;12(1):10910.
- Berger SE, Baria AT. Assessing Pain Research: A Narrative Review of Emerging Pain Methods, Their Technosocial Implications, and Opportunities for Multidisciplinary Approaches. Front Pain Res (Lausanne) 2022;3:896276.
- 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.
- Fisher AS, Lanigan MT, Upton N, Lione LA. Preclinical Neuropathic Pain Assessment; the Importance of Translatability and Bidirectional Research. Front Pharmacol 2020;11:614990.
- Maskato Y, Dugdale AHA, Singer ER, Kelmer G, Sutton GA. Prospective Feasibility and Revalidation of the Equine Acute Abdominal Pain Scale (EAAPS) in Clinical Cases of Colic in Horses. Animals (Basel) 2020 Nov 29;10(12).
- 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.
- 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 (Basel) 2020 Oct 9;10(10).
- Cohen S, Beths T. Grimace Scores: Tools to Support the Identification of Pain in Mammals Used in Research. Animals (Basel) 2020 Sep 23;10(10).
- Hohlbaum K, Corte GM, Humpenöder M, Merle R, Thöne-Reineke C. Reliability of the Mouse Grimace Scale in C57BL/6JRj Mice. Animals (Basel) 2020 Sep 14;10(9).
- de Camp NV, Ladwig-Wiegard M, Geitner CIE, Bergeler J, Thöne-Reineke C. EEG based assessment of stress in horses: a pilot study. PeerJ 2020;8:e8629.
- 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 (Basel) 2020 Apr 30;10(5).
- Andresen N, Wöllhaf M, Hohlbaum K, Lewejohann L, Hellwich O, Thöne-Reineke C, Belik V. Towards a fully automated surveillance of well-being status in laboratory mice using deep learning: Starting with facial expression analysis. PLoS One 2020;15(4):e0228059.
- 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).
- Jirkof P, Rudeck J, Lewejohann L. Assessing Affective State in Laboratory Rodents to Promote Animal Welfare-What Is the Progress in Applied Refinement Research?. Animals (Basel) 2019 Nov 25;9(12).
- Tappe-Theodor A, King T, Morgan MM. Pros and Cons of Clinically Relevant Methods to Assess Pain in Rodents. Neurosci Biobehav Rev 2019 May;100:335-343.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists