Competition and stereotypic behavior in Thoroughbred horses: The value of saliva as a diagnostic marker of stress.
Abstract: Many horses exhibit stereotypies, especially when living in human controlled environments that may prevent horses from satisfying natural needs in terms of feeding, drinking, moving, and socializing. In human medicine, obsessive compulsive disorder and other severe psychiatric disturbances are associated with stereotypic behaviors; salivary biomarkers evaluation is considered a reliable tool for diagnosis of common mental health disorders because saliva collection easy to obtain and noninvasive. In this study, we hypothesized that salivary cortisol concentrations, in addition to alpha-amylase (sAA) and butyrylcholinesterase (BChE) activities, are considered stress biomarkers that may be influenced in horses trained for racing competition with stereotypic behaviors. Saliva at rest condition was obtained from ten non-stereotypic Thoroughbreds horses involved in high-level competition; eleven Thoroughbreds high-level competition horses showing stereotypic behaviors, and five Thoroughbreds leisure non-competition horses. Cortisol was found to be higher in high-level competition non-stereotypic horses and sAA was significantly higher in non-stereotypic leisure horses when compared to horses involved in competition, while BChE did not change between groups. These results may represent the basis for further behavioural evaluation to elucidate how stereotypic horses and horses involved in competition overcome stressful situations.
Copyright: © 2024 Bazzano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Publication Date: 2024-10-07 PubMed ID: 39374248PubMed Central: PMC11458048DOI: 10.1371/journal.pone.0311697Google 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
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 article studies the correlation between stress-induced behaviors in Thoroughbred horses and the biomarkers present in their saliva. The focus of the study is to assess whether specific biomarker concentrations are influenced by competitive training and stereotypic behaviors commonly seen in race horses.
Objective of the Study
- The goal of the study is to investigate whether salivary cortisol concentrations, alpha-amylase (sAA) activities, and butyrylcholinesterase (BChE) activities are useful stress indicators in Thoroughbred horses exhibiting stereotypic behaviors while being trained for high-level competition.
Methodology and Participants
- For this study, three groups of Thoroughbreds were compiled: ten involved in high-level competition but with no stereotypies, eleven involved in high-level competition with stereotypic behaviors, and five that were non-competitive leisure horses.
- At a resting condition, the horses’ saliva was collected and analyzed for salivary cortisol, sAA and BChE.
Findings of the Study
- The horses used in high-level competition without stereotypies had higher cortisol levels compared to their counterparts.
- Non-competitive leisure horses, which did not exhibit stereotypic behaviors, were found to have significantly higher sAA levels compared to the horses used in high-level competition.
- No significant changes were recorded in the BChE levels among the different groups of horses.
Implications of the Findings
- The findings from this study lay the groundwork for further behavioral evaluations that may help in understanding how horses with stereotypic behaviors and race horses cope with stress.
- Furthermore, these results indicate the potential utility of salivary biomarkers as noninvasive diagnostic tools in evaluating stress levels in horses, similar to the application in human medicine for diagnosing mental health disorders.
Cite This Article
APA
Bazzano M, Marchegiani A, La Gualana F, Petriti B, Petrucelli M, Accorroni L, Laus F.
(2024).
Competition and stereotypic behavior in Thoroughbred horses: The value of saliva as a diagnostic marker of stress.
PLoS One, 19(10), e0311697.
https://doi.org/10.1371/journal.pone.0311697 Publication
Researcher Affiliations
- School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
- School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
- Department of Translational and Precision Medicine, Sapienza, University of Rome, Rome, Italy.
- Department of Translational and Precision Medicine, Sapienza, University of Rome, Rome, Italy.
- School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
- School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
- School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
MeSH Terms
- Animals
- Horses
- Saliva / chemistry
- Saliva / metabolism
- Hydrocortisone / analysis
- Hydrocortisone / metabolism
- Stereotyped Behavior / physiology
- Biomarkers / metabolism
- Biomarkers / analysis
- Behavior, Animal / physiology
- Male
- Butyrylcholinesterase / metabolism
- Female
- Stress, Psychological / metabolism
- alpha-Amylases / metabolism
- Competitive Behavior / physiology
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 44 references
- Mason G, Rushen J. Stereotypic animal behaviour: fundamentals and applications to welfare. 2nd Edition. CABI Pub.; 2006.
- Overall KL. Pharmacological approaches to changing behavior and neurochemistry: roles for diet, supplements, nutraceuticals, and medication. Manual of clinical behavioral medicine for dogs and cats Elsevier Mosby, editor. 2013; 458–512.
- Mason GJ. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare and beyond. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2008; 367.
- Carroll SL, Sykes BW, Mills PC. Understanding and treating equine behavioural problems. The Veterinary Journal 2023;296–297: 105985.
- Hanis F, Chung ELT, Kamalludin MH, Idrus Z. The Influence of Stable Management and Feeding Practices on the Abnormal Behaviors Among Stabled Horses in Malaysia. J Equine Vet Sci 2020;94.
- Hanis F, Chung ELT, Kamalludin MH, Idrus Z. Discovering the relationship between dietary nutrients and cortisol and ghrelin hormones in horses exhibiting oral stereotypic behaviors: A review. Journal of Veterinary Behavior 2020;39: 90–98.
- Moberg GP, Mench JA. The biology of animal stress: basic principles and implications for animal welfare. 2000 [cited 15 May 2024].
- Nagy K, Bodó G, Bárdos G, Bánszky N, Kabai P. Differences in temperament traits between crib-biting and control horses. Appl Anim Behav Sci 2010;122: 41–47.
- Clegg HA, Buckley P, Friend MA, McGreevy PD. The ethological and physiological characteristics of cribbing and weaving horses. Appl Anim Behav Sci 2008;109: 68–76.
- Sarrafchi A, Blokhuis HJ. Equine stereotypic behaviors: Causation, occurrence, and prevention. 2013 [cited 15 May 2024].
- Nicol C. Understanding equine stereotypies. Equine Vet J 1999;31: 20–25.
- Hausberger M, Gautier E, Biquand V, Lunel C, Jégo P. Could Work Be a Source of Behavioural Disorders? A Study in Horses. PLoS One 2009;4.
- Briefer Freymond S, Ruet A, Grivaz M, Fuentes C, Zuberbühler K, Bachmann I. Stereotypic horses (Equus caballus) are not cognitively impaired. Anim Cogn 2019;22: 17–33.
- Briefer Freymond S, Beuret S, Ruet A, Zuberbühler K, Bachmann I, Briefer EF. Stereotypic behaviour in horses lowers stress but not spatial learning performance. Appl Anim Behav Sci 2020;232.
- McBride SD, Cí·¯ord D. The Putative Welfare-Reducing Effects of Preventing Equine Stereotypic Behaviour. Animal Welfare 2001;10: 173–189.
- Hyvärinen E, Kashyap B, Kullaa AM. Oral Sources of Salivary Metabolites. Metabolites 2023;13.
- Bazzano M, Laghi L, Zhu C, Lotito E, Sgariglia S, Tesei B. Exercise Induced Changes in Salivary and Serum Metabolome in Trained Standardbred, Assessed by 1H-NMR. Metabolites 2020;10: 1–14.
- Tuttolomondo D, Antonelli R, Setti G, Ardissino D, Pertinhez T, Gallo M. Salivary biomarkers for diagnosis of acute myocardial infarction: A systematic review. Int J Cardiol 2023;371: 54–64.
- Chojnowska S, Ptaszyńska-Sarosiek I, Kępka A, Knaś M, Waszkiewicz N. Salivary Biomarkers of Stress, Anxiety and Depression. Journal of Clinical Medicine 2021;10: 517.
- Shih P an (Betty). Metabolomics Biomarkers for Precision Psychiatry. Adv Exp Med Biol 2019;1161: 101.
- Nater UM, Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 2009;34: 486–496.
- Strahler J, Skoluda N, Kappert MB, Nater UM. Simultaneous measurement of salivary cortisol and alpha-amylase: Application and recommendations. Neurosci Biobehav Rev 2017;83: 657–677.
- Sánchez-Amate MC, Flores P, Sánchez-Santed F. Effects of chlorpyrifos in the plus-maze model of anxiety. Behavioural pharmacology 2001;12: 285–292.
- Archana E, Pai P, Prabhu BK, Shenoy RP, Prabhu K, Rao A. Altered biochemical parameters in saliva of pediatric attention deficit hyperactivity disorder. Neurochem Res 2012;37: 330–334.
- Fureix C, Benhajali H, Henry S, Bruchet A, Prunier A, Ezzaouia M. Plasma cortisol and faecal cortisol metabolites concentrations in stereotypic and non-stereotypic horses: Do stereotypic horses cope better with poor environmental conditions?. BMC Vet Res 2013;9: 1–10.
- Sikorska U, Maśko M, Ciesielska A, Zdrojkowski Ł, Domino M. Role of Cortisol in Horse’s Welfare and Health. Agriculture 2023;13: 2219.
- Pell SM, McGreevy PD. A study of cortisol and beta-endorphin levels in stereotypic and normal Thoroughbreds. Appl Anim Behav Sci 1999;64: 81–90.
- Hemmann K, Raekallio M, Kanerva K, Hänninen L, Pastell M, Palviainen M. Circadian variation in ghrelin and certain stress hormones in crib-biting horses. Vet J 2012;193: 97–102.
- Contreras-Aguilar MD, Henry S, Coste C, Tecles F, Escribano D, Cerón JJ. Changes in saliva analytes correlate with horses’ behavioural reactions to an acute stressor: A pilot study. Animals 2019;9.
- Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares. Equine Vet J 1983;15: 371–372.
- Contreras-Aguilar MD, Hevia ML, Escribano D, Lamy E, Tecles F, Cerón JJ. Effect of food contamination and collection material in the measurement of biomarkers in saliva of horses. Res Vet Sci 2020;129: 90–95.
- Malamud D, Rodriguez-Chavez IR. Saliva as a Diagnostic Fluid. Dent Clin North Am 2011;55: 159.
- McGreevy P, Nicol C. Physiological and behavioral consequences associated with short-term prevention of crib-biting in horses. Physiol Behav 1998;65: 15–23.
- Bachmann I, Bernasconi P, Herrmann R, Weishaupt MA, Staᆲher M. Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Appl Anim Behav Sci 2003;82: 297–311.
- Massányi M, Halo M, Mlyneková E, Kováčiková E, Tokárová K, Greń A. The effect of training load stress on salivary cortisol concentrations, health parameters and hematological parameters in horses. Heliyon 2023;9.
- Kułak-Bejda A, Waszkiewicz N, Bejda G, Zalewska A, Maciejczyk M. Diagnostic Value of Salivary Markers in Neuropsychiatric Disorders. Dis Markers 2019;2019.
- Freymond SB, Bardou D, Beuret S, Bachmann I, Zuberbühler K, Briefer EF. Elevated sensitivity to tactile stimuli in stereotypic horses. Front Vet Sci 2019;6: 443655.
- Briefer Freymond S, Bardou D, Briefer EF, Bruckmaier R, Fouché N, Fleury J. The physiological consequences of crib-biting in horses in response to an ACTH challenge test. Physiol Behav 2015;151: 121–128.
- Aurich J, Wulf M, Ille N, Erber R, von Lewinski M, Palme R. Effects of season, age, sex, and housing on salivary cortisol concentrations in horses. Domest Anim Endocrinol 2015;52: 11–16.
- Contreras-Aguilar M, Escribano D, Martínez-Subiela S, Martín-Cuervo M, Lamy E, Tecles F. Changes in saliva analytes in equine acute abdominal disease: a sialochemistry approach. BMC Vet Res 2019;15.
- Schrödl W, Büchler R, Wendler S, Reinhold P, Muckova P, Reindl J. Acute phase proteins as promising biomarkers: Perspectives and limitations for human and veterinary medicine. Proteomics Clin Appl 2016;10: 1077–1092.
- Kusmawan D, Rini WNE, Aurora WID. Relation of Salivary Alpha-Amylase (sAA) Concentration to Fatigue Biomarkers in Palm Oil Office Workers in Jambi Province: Preliminary Study. Makara J Sci 2023;27: 289–297.
- Contreras-Aguilar MD, Cerón JJ, Muñoz A, Ayala I. Changes in saliva biomarkers during a standardized increasing intensity field exercise test in endurance horses. Animal 2021;15.
- Bazzano M, Marchegiani A, La Gualana F, Petriti B, Spaterna A, Laus F. Salivary analysis to unveil the paradigma of stress of domestic horses reared in the wild. Sci Rep 2024;14: 11266.
Citations
This article has been cited 0 times.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