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PloS one2024; 19(10); e0311697; doi: 10.1371/journal.pone.0311697

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.
Publication Date: 2024-10-07 PubMed ID: 39374248PubMed Central: PMC11458048DOI: 10.1371/journal.pone.0311697Google Scholar: Lookup
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  • Journal Article

Summary

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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

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 19
Issue: 10
Pages: e0311697
PII: e0311697

Researcher Affiliations

Bazzano, Marilena
  • School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
Marchegiani, Andrea
  • School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
La Gualana, Francesca
  • Department of Translational and Precision Medicine, Sapienza, University of Rome, Rome, Italy.
Petriti, Begi
  • Department of Translational and Precision Medicine, Sapienza, University of Rome, Rome, Italy.
Petrucelli, Marina
  • School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
Accorroni, Lucrezia
  • School of Biosciences and Veterinary Medicine, University of Camerino, Matelica, Italy.
Laus, Fulvio
  • 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
  1. Mason G, Rushen J. Stereotypic animal behaviour: fundamentals and applications to welfare. 2nd Edition. CABI Pub.; 2006.
  2. 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.
  3. Mason GJ. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare and beyond. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2008; 367.
  4. Carroll SL, Sykes BW, Mills PC. Understanding and treating equine behavioural problems. The Veterinary Journal 2023;296–297: 105985.
    doi: 10.1016/j.tvjl.2023.105985pubmed: 37127134google scholar: lookup
  5. 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.
    doi: 10.1016/j.jevs.2020.103230pubmed: 33077069google scholar: lookup
  6. 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.
  7. Moberg GP, Mench JA. The biology of animal stress: basic principles and implications for animal welfare. 2000 [cited 15 May 2024].
  8. 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.
  9. 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.
  10. Sarrafchi A, Blokhuis HJ. Equine stereotypic behaviors: Causation, occurrence, and prevention. 2013 [cited 15 May 2024].
  11. Nicol C. Understanding equine stereotypies. Equine Vet J 1999;31: 20–25.
  12. 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.
  13. 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.
    doi: 10.1007/s10071-018-1217-8pubmed: 30328528google scholar: lookup
  14. 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.
  15. McBride SD, Cí·¯ord D. The Putative Welfare-Reducing Effects of Preventing Equine Stereotypic Behaviour. Animal Welfare 2001;10: 173–189.
    doi: 10.1017/S0962728600023848google scholar: lookup
  16. Hyvärinen E, Kashyap B, Kullaa AM. Oral Sources of Salivary Metabolites. Metabolites 2023;13.
    doi: 10.3390/metabo13040498pmc: PMC10145445pubmed: 37110157google scholar: lookup
  17. 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.
    doi: 10.3390/METABO10070298pmc: PMC7407172pubmed: 32708237google scholar: lookup
  18. 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.
    doi: 10.1016/j.ijcard.2022.09.043pubmed: 36167219google scholar: lookup
  19. 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.
    doi: 10.3390/jcm10030517pmc: PMC7867141pubmed: 33535653google scholar: lookup
  20. Shih P an (Betty). Metabolomics Biomarkers for Precision Psychiatry. Adv Exp Med Biol 2019;1161: 101.
  21. 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.
  22. 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.
  23. Sánchez-Amate MC, Flores P, Sánchez-Santed F. Effects of chlorpyrifos in the plus-maze model of anxiety. Behavioural pharmacology 2001;12: 285–292.
  24. 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.
    doi: 10.1007/s11064-011-0616-xpubmed: 21964765google scholar: lookup
  25. 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.
  26. Sikorska U, Maśko M, Ciesielska A, Zdrojkowski Ł, Domino M. Role of Cortisol in Horse’s Welfare and Health. Agriculture 2023;13: 2219.
  27. 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.
  28. 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.
    doi: 10.1016/j.tvjl.2011.09.027pubmed: 22040804google scholar: lookup
  29. 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.
    doi: 10.3390/ani9110993pmc: PMC6912570pubmed: 31752194google scholar: lookup
  30. 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.
  31. 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.
    doi: 10.1016/j.rvsc.2020.01.006pubmed: 31954319google scholar: lookup
  32. Malamud D, Rodriguez-Chavez IR. Saliva as a Diagnostic Fluid. Dent Clin North Am 2011;55: 159.
    doi: 10.1016/j.cden.2010.08.004pmc: PMC3011946pubmed: 21094724google scholar: lookup
  33. McGreevy P, Nicol C. Physiological and behavioral consequences associated with short-term prevention of crib-biting in horses. Physiol Behav 1998;65: 15–23.
    doi: 10.1016/s0031-9384(98)00070-5pubmed: 9811360google scholar: lookup
  34. 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.
  35. 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.
  36. Kułak-Bejda A, Waszkiewicz N, Bejda G, Zalewska A, Maciejczyk M. Diagnostic Value of Salivary Markers in Neuropsychiatric Disorders. Dis Markers 2019;2019.
    doi: 10.1155/2019/4360612pmc: PMC6525852pubmed: 31191750google scholar: lookup
  37. 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.
  38. 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.
    doi: 10.1016/j.physbeh.2015.07.015pubmed: 26187578google scholar: lookup
  39. 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.
  40. 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.
    doi: 10.1186/s12917-019-1933-6pmc: PMC6554884pubmed: 31170977google scholar: lookup
  41. 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.
    doi: 10.1002/prca.201600028pubmed: 27274000google scholar: lookup
  42. 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.
    doi: 10.7454/mss.v27i4.1450google scholar: lookup
  43. 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.
    doi: 10.1016/j.animal.2021.100236pubmed: 34030029google scholar: lookup
  44. 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.
    doi: 10.1038/s41598-024-62172-2pmc: PMC11101484pubmed: 38760454google scholar: lookup

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