FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Low plasma cortisol and fecal cortisol metabolite measures a...
PloS one2017; 12(9); e0182257; doi: 10.1371/journal.pone.0182257

Low plasma cortisol and fecal cortisol metabolite measures as indicators of compromised welfare in domestic horses (Equus caballus).

Abstract: The hypothalamic-pituitary-adrenal (HPA) axis response to chronic stress is far from straight forward, particularly with regards to animal welfare. There are reports of no effect as well as both decreases and increases in cortisol after chronic stressors. Therefore, the first aim of the present study was to determine how measures of compromised welfare, such as chronic pain and haematological anomalies, related to cortisol levels in domestic horses (Equus caballus). Domestic horses are an informative model to investigate the impact of chronic stress (due to environment, pain, work, housing conditions…) on the HPA axis. The second aim was to determine whether levels of fecal cortisol metabolites (FCM) may be used as an indicator of welfare measures. The present study used fifty-nine horses (44 geldings and 15 mares), from three riding centres in Brittany, France. The primary findings show that horses whose welfare was clearly compromised (as indicated by an unusual ears backward position, presence of vertebral problems or haematological anomalies, e.g. anaemia) also had lower levels of both FCM and plasma cortisol. This work extends our previous findings showing that withdrawn postures, indicators of depressive-like behavior in horses, are associated with lower plasma cortisol levels. We also found that evening plasma cortisol levels positively correlated with FCM levels in horses. Future research aims to determine the extent to which factors of influence on welfare, such as living conditions (e.g. single stalls versus group housing in pasture or paddocks), early life factors, and human interaction, act as mediators of cortisol levels in horses.
Get Full Text
Publication Date: 2017-09-08 PubMed ID: 28886020PubMed Central: PMC5590897DOI: 10.1371/journal.pone.0182257Google 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

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 focuses on the relationship between cortisol levels and the welfare of domestic horses, investigating whether lower levels of cortisol, as reflected in plasma and fecal samples, might indicate compromised welfare resulting from chronic stress, pain, or anomalies like anemia.

Overview of the Study

  • The study revolves around the understanding of the hypothalamic-pituitary-adrenal (HPA) axis’ response to chronic stress, particularly in the context of domestic horses. The response to chronic stress is complex and can vary significantly, with reported findings including no effect, decreases, and increases in cortisol levels following chronic stressors.
  • This research specifically sought to explore the possible links between measures indicative of compromised welfare, such as chronic pain and haematological anomalies, and cortisol levels in domestic horses (Equus caballus).
  • Domestic horses were chosen as the model for the study because their circumstances often include a variety of chronic stressors such as environmental factors, pain, workload, and various housing conditions.

Aims of the Study

  • The first aim of the study was to draw a conclusive correlation between chronic stressors and their impact on cortisol levels in horses. This was to ascertain whether chronic stressors led to an increase, decrease, or had no effect on cortisol levels.
  • The second objective of the study was to determine if fecal cortisol metabolites (FCM) could be used as an accurate indicator of welfare measures, offering another means of monitoring stress levels in horses.

Design and Results of the Study

  • The study was conducted using fifty-nine horses from three riding centres in Brittany, France. The selection consisted of 44 geldings and 15 mares.
  • The findings of the study showed that horses with compromised welfare – as indicated by unusual ear positions, vertebral problems, or haematological anomalies such as anaemia – also demonstrated lower levels of both plasma cortisol and fecal cortisol metabolites (FCMs).
  • The study found a positive correlation between evening plasma cortisol levels and FCM levels in horses, suggesting a relationship between the two.

Implications and Future Research

  • The study fortifies previous findings of the relationship between lower plasma cortisol levels and behaviours indicative of depression in horses, such as withdrawn postures.
  • The study sets the stage for future research to explore how other factors that influence welfare – like living conditions (single stalls versus group housing), early life factors, and human interaction – further influence cortisol levels in horses, thus affecting their welfare adversely or otherwise.

Cite This Article

APA
Pawluski J, Jego P, Henry S, Bruchet A, Palme R, Coste C, Hausberger M. (2017). Low plasma cortisol and fecal cortisol metabolite measures as indicators of compromised welfare in domestic horses (Equus caballus). PLoS One, 12(9), e0182257. https://doi.org/10.1371/journal.pone.0182257

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 12
Issue: 9
Pages: e0182257

Researcher Affiliations

Pawluski, Jodi
  • Institut de recherche en santé, environnement et travail (Irset), U1085 INSERM, Université de Rennes 1, Rennes, France.
Jego, Patrick
  • Université de Rennes 1, UMR 6552 CNRS Ethologie Animale et Humaine, Station Biologique de Paimpont, France.
Henry, Séverine
  • Université de Rennes 1, UMR 6552 CNRS Ethologie Animale et Humaine, Station Biologique de Paimpont, France.
Bruchet, Anaelle
  • Université de Rennes 1, UMR 6552 CNRS Ethologie Animale et Humaine, Station Biologique de Paimpont, France.
Palme, Rupert
  • University of Veterinary Medicine, Department of Biomedical Sciences, Vienna, Austria.
Coste, Caroline
  • Université de Rennes 1, UMR 6552 CNRS Ethologie Animale et Humaine, Station Biologique de Paimpont, France.
Hausberger, Martine
  • CNRS, UMR 6552 Ethologie animale et humaine, Université de Rennes 1, Rennes, France.

MeSH Terms

  • Animal Welfare / standards
  • Animals
  • Biomarkers
  • Blood Cell Count
  • Erythrocyte Indices
  • Feces / chemistry
  • Female
  • Horses
  • Hydrocortisone / blood
  • Hydrocortisone / metabolism
  • Stress, Physiological
  • Stress, Psychological / blood
  • Stress, Psychological / metabolism

Conflict of Interest Statement

Competing Interests: The authors have declared that no competing interests exist.

References

This article includes 104 references
  1. von Borell E. Neuroendocrine integration of stress and significance of stress for the performance of farm animals. Applied Animal Behaviour Science 1995;44:219–27.
  2. Palme R, Rettenbacher S, Touma C, El-Bahr S, Möstl E. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion and noninvasive measurement in fecal samples. Annals New York Acad Sci 2005;1040:162–71.
    pubmed: 15891021
  3. Palme R. Measuring fecal steroids—Guidelines for practical application. Bird Hormones and Bird Migrations: Analyzing Hormones in Droppings and Egg Yolks and Assessing Adaptations in Long-Distance Migration 2005;1046:75–80.
    doi: 10.1196/annals.1343.007pubmed: 16055844google scholar: lookup
  4. Mormede P, Andanson S, Auperin B, Beerda B, Guemene D, Malnikvist J. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 2007;92(3):317–39.
    doi: 10.1016/j.physbeh.2006.12.003pubmed: 17234221google scholar: lookup
  5. Dickens MJ, Romero LM. A consensus endocrine profile for chronically stressed wild animals does not exist. General and comparative endocrinology 2013;191:177–89.
    doi: 10.1016/j.ygcen.2013.06.014pubmed: 23816765google scholar: lookup
  6. Rushen J. Problems associated with the interpretation of physiological data in the assessment of animal-welfare. Applied Animal Behaviour Science 1991;28:381–6.
  7. Miller GE, Chen E, Zhou ES. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin 2007;133(1):25–45.
    doi: 10.1037/0033-2909.133.1.25pubmed: 17201569google scholar: lookup
  8. Michaud K, Matheson K, Kelly O, Anisman H. Impact of stressors in a natural context on release of cortisol in healthy adult humans: A meta-analysis. Stress-the International Journal on the Biology of Stress 2008;11(3):177–97.
    doi: 10.1080/10253890701727874pubmed: 18465466google scholar: lookup
  9. Munksgaard L, Simonsen HB. Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down. Journal of Animal Science 1996;74:769–78.
    pubmed: 8727997
  10. Veissier I, Chazal P, Pradel P, LeNeindre P. Providing social contacts and objects for nibbling moderates reactivity and oral behaviors in veal calves. Journal of Animal Science 1997;75:356–65.
    pubmed: 9051458
  11. Casamassima D, Sevi A, Palazzo M, Ramacciato R, Colella GE, Bellitti A. Effects of two different housing systems on behavior, physiology and milk yield of Comisana ewes. Small Ruminant Research 2001;41:151–61.
    pubmed: 11445423
  12. Otten W, Kanitz E, Puppe B, Tuchscherer M, Brussow KP, Nurnberg G. Acute and long term effects of chronic intermittent noise stress on hypothalamic-pituitary-adrenocortical and sympathoadrenomedullary axis in pigs. Animal Science 2004;78:271–83.
  13. Kanitz E, Otten W, Tuchscherer M. Central and peripheral effects of repeated noise stress on hypothalamic-pituitary-adrenocortical axis in pigs. Livestock Production Science 2005;94:213–24.
  14. deJonge FH, Bokkers EAM, Schouten WGP, Helmond FA. Rearing piglets in a poor environment: Developmental aspects of social stress in pigs. Physiology & Behavior 1996;60:389–96.
    pubmed: 8840896
  15. Meunier-Salaün MC, Vantrimponte MN, Raab A, Dantzer R. Effect of floor area restriction upon performance, behavior and physiology of growing-finishing pigs. Journal of Animal Science 1987;64:1371–7.
    pubmed: 3583943
  16. Barnett JL, Hemsworth PH, Cronin GM, Newman EA, McCallum TH, Chilton D. Effects of pen size, partial stalls and method of feeding on welfare-related behavioral and physiological-responses of group-housed pig. Applied Animal Behaviour Science 1992;34:207–20.
  17. Pearce GP, Paterson AM. The effect of space restriction and provision of toys during rearing on the behavior, productivity and physiology of male pigs. Applied Animal Behaviour Science 1993;36:11–28.
  18. Van Reenen CG, Mars MH, Leushuis IE, Rijsewijk FA, van Oirschot JT, Blokhuis HJ. Social isolation may influence responsiveness to infection with bovine herpes virus 1 in veal calves. Veterinary Microbiology 2000;75:135–43.
    pubmed: 10889404
  19. Ladewig J, Smidt D. Behavior, episodic secretion of cortisol, and adrenocortical reactivity in bulls subjected to tethering. Hormones and Behavior 1989;23(3):344–60.
    pubmed: 2793077
  20. Fisher AD, Crowe MA, Prediville DJ, Enright WJ. Indoor space allowance: Effects on growth, behavior, adrenal and immune responses of finishing beef heifers. Animal Science 1997;64:53–62.
  21. Cyr NE, Michael Romero L. Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. General and comparative endocrinology 2007;151(1):82–9.
    doi: 10.1016/j.ygcen.2006.12.003pubmed: 17280663google scholar: lookup
  22. Jensen KH, Pedersen LJ, Nielsen EK, Heller KE, Ladewig J, Jorgensen E. Intermittent stress in pigs: Effects on behavior, pituitary-adrenocortical axis, growth, and gastric ulceration. Physiology & Behavior 1996;59(4–5):741–8.
    pubmed: 8778861
  23. Houpt K, Houpt TR, Johnson JL, Erb HN, Yeon SC. The Effect of Exercise Deprivation on the Behaviour and Physiology of Straight Stall Confined Pregnant Mares. Animal Welfare 2001;10(3):257–67.
  24. Visser EK, Ellis AD, Van Reenen CG. The effect of two different housing conditions on the welfare of young horses stabled for the first time. Applied Animal Behaviour Science 2008;114(3–4):521–33.
    doi: 10.1016/j.applanim.2008.03.003google 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 veterinary research 2013;9:3.
    doi: 10.1186/1746-6148-9-3pmc: PMC3544618pubmed: 23289406google scholar: lookup
  26. Fureix C, Jego P, Henry S, Lansade L, Hausberger M. Towards an ethological animal model of depression? A study on horses. PloS one 2012;7(6):e39280.
    doi: 10.1371/journal.pone.0039280pmc: PMC3386251pubmed: 22761752google scholar: lookup
  27. Broom DM. Animal welfare: concepts and measurement. J AnimSci 1991;69:4167–75.
    pubmed: 1778832
  28. Dawkins MS. From an animal's point of view: Motivation, fitness, and animal welfare. Behavioral and Brain Sciences 1990;13:1–61.
  29. Fraser D. Assessing animal well-being: common sense, uncommon science. The Proceedings of the Conference on Food Animal Well-Being West Lafayette, IN: USDA and Purdue University, Office of Agriculture Research for Programs 1993. p. 37–54.
  30. Blokhuis HJ, Jones RB, Geers R, Miele M, Veissier I. Measuring and monitoring animal welfare: transparency in the food product quality chain. Animal Welfare 2003;12(4):445–55.
  31. Mills DS. Repetitive movement problems in the horse. The Domestic Horse: The Origins, Development and Management of its Behaviour: Cambridge University Press 2005. p. 212–27.
  32. Hausberger M, Gautier E, Biquand V, Lunel C, Jego P. Could work be a source of behavioural disorders? A study in horses. PloS one 2009;4(10):e7625.
    doi: 10.1371/journal.pone.0007625pmc: PMC2763287pubmed: 19862328google scholar: lookup
  33. Hausberger M, Gautier R, Muller C, Jego P. Lower learning abilities in stereotypic horses. Applied Animal Behaviour Science 2007;107(3–4):299–306.
  34. Hausberger M, Fureix C, Lesimple C. Detecting horses’ sickness: in search of visible signs. Applied Animal Behaviour Science 2016;175:41–9.
  35. McGreevy P, Cripps P, French N, Green L, Nicol C. Managementfactors associated with stereotypic and redirected behavior in thethoroughbred horse. Equine Veterinary Journal 1995;27:86–91.
    pubmed: 7607155
  36. Fureix C, Hausberger M, Seneque E, Morisset S, Baylac M, Cornette R. Geometric morphometrics as a tool for improving the comparative study of behavioural postures. Die Naturwissenschaften 2011;98(7):583–92.
    doi: 10.1007/s00114-011-0803-2pubmed: 21573691google scholar: lookup
  37. Lesimple C, Fureix C, De Margerie E, Seneque E, Menguy H, Hausberger M. Towards a postural indicator of back pain in horses (Equus caballus). PloS one 2012;7(9):e44604.
    doi: 10.1371/journal.pone.0044604pmc: PMC3436792pubmed: 22970261google scholar: lookup
  38. Lesimple C, Fureix C, Menguy H, Hausberger M. Human direct actions may alter animal welfare, a study on horses (Equus caballus). PloS one 2010;5(4):e10257.
    doi: 10.1371/journal.pone.0010257pmc: PMC2860978pubmed: 20442766google scholar: lookup
  39. Fureix C, Menguy H, Hausberger M. Partners with bad temper: reject or cure? A study of chronic pain and aggression in horses. PloS one 2010;5(8):e12434.
    doi: 10.1371/journal.pone.0012434pmc: PMC2928779pubmed: 20865160google scholar: lookup
  40. Fureix C, Meagher RK. What can inactivity (in its various forms) reveal about affective states in non-human animals? A review. Applied Animal Behaviour Science 2015;171:8–24.
    doi: 10.1016/j.applanim.2015.08.036google scholar: lookup
  41. Burn CC, Dennison TL, Whay HR. Environmental and demographic riskfactors for poor welfare in working horses: donkeys and mules in developingcountries. Vet J 2010;186:385–92.
    doi: 10.1016/j.tvjl.2009.09.016pubmed: 19926316google scholar: lookup
  42. Lesimple C, Fureix C, Aube L, Hausberger M. Detecting horses' sickness: the example of back disorders. Applied Animal Behaviour Science 2016.
  43. Lesimple C, Aube L, Fureix C, Hausberger M. Detecting and Measuring Back Disorders in Nonverbal Individuals: The Example of Domestic Horses. Animal Behavior and Cognition 2016;3(3):159–79.
    doi: 10.12966/abc.05.08.2016google scholar: lookup
  44. Lesimple C, Fureix C, Biquand V, Hausberger M. Comparison of clinical examinations of back disorders and humans' evaluation of back pain in riding school horses. BMC veterinary research 2013;9:209.
    doi: 10.1186/1746-6148-9-209pmc: PMC4015870pubmed: 24128080google scholar: lookup
  45. Fonseca BPA, Alves ALG, Nicoletti JLM, Thornassian A, Hussni CA, Mikail S. Thermography and ultrasonography in back pain diagnosis of equine athletes. Journal of Equine Veterinary Science 2006;26(11):507–16.
    doi: 10.1016/j.jevs.2006.09.007google scholar: lookup
  46. Benhajali H, Ezzaouia M, Lunel C, Charfi F, Hausberger M. Stereotypic behaviours and mating success in domestic mares. Appl Anim Behav Sci 2014;153:36–42.
  47. Nicol CJ, Davidson HPD, Harris PA, Waters AJ, Wilson AD. Study of crib-biting and gastric inflammation and ulceration in young horses. Vet Rec 2002;151:658–62.
    pubmed: 12498408
  48. Cooper J, McGreevy P. Stereotypic Behaviour in the Stabled Horse: Causes, Effects and Prevention without Compromising Horse Welfare. The Welfare of Horses. Animal Welfare 1: Springer; 2007. p. 99–124.
  49. Goodwin D. Horse Behaviour: Evolution, Domestication and Feralisation. The Welfare of Horses 1: Springer; 2007. p. 1–18.
  50. Harris P. How should we feed horses- and how many times a day?. Vet J 2007;173:252–3.
    pubmed: 17393570
  51. Sankey C, Richard-Yris MA, Henry S, Fureix C, Nassur F, Hausberger M. Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Animal cognition 2010;13(5):753–64.
    doi: 10.1007/s10071-010-0326-9pubmed: 20490592google scholar: lookup
  52. Normando S, Meers L, Samuels WE, Faustini M, Odberg FO. Variables affecting the prevalence of behavioural problems in horses. Can riding style and other management factors be significant?. Appl Anim Behav Sci 2011;133:186–98.
  53. Visser EK, Neijenhuis F, De Graff-Roelfseman E, Wesselink HGM, de Boer J, van Wijhe-Kiezebrink MC. Risk factors associated with health disorders in sport and leisure horses in the Netherlands. Journal of Animal Science 2014;92:844–55.
    doi: 10.2527/jas.2013-6692pubmed: 24352963google scholar: lookup
  54. Hausberger M, Muller C, Lunel C. Does work affect personality? A study in horses. PloS one 2011;6(2):e14659.
    doi: 10.1371/journal.pone.0014659pmc: PMC3036583pubmed: 21347405google scholar: lookup
  55. Mostl E, Messmann S, Bagu E, Robia C, Palme R. Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Zentralbl Veterinarmed A 1999;46(10):621–31.
    pubmed: 10638300
  56. Merl S, Scherzer S, Palme R, Möstl E. Pain causes increased concentrations of glucocorticoid metabolites in horse feces. J Equine Vet Sci 2000;20:586–90.
  57. Palme R. Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals. Animal Welfare 2012;21:331–7.
  58. Lesimple C, Poissonnet A, Hausberger M. How to keep your horse safe? An epidemiological study about management practices. Applied Animal Behaviour Science 2016.
  59. Hoffsis GF, Murdick PW, Tharp VL, Ault K. Plasma concentrations of cortisol and corticosterone in normal horse. American Journal of Veterinary Research 1970;31(8):1379–&.
    pubmed: 4317816
  60. James VHT, Horner MW, Moss MS, Rippon AE. Adrenocortical function in horse. Journal of Endocrinology 1970;48(3):319–&.
    pubmed: 4320413
  61. Bottoms GD, Akins EL, Rausch FD, Roesel OF. Circadian variation in plasma cortisol and corticosterone in pigs and mares. American Journal of Veterinary Research 1972;33(4):785–&.
    pubmed: 5017871
  62. Kirkpatrick JF, Wiesner L, Baker CB, Angle M. Diurnal- variation of plasma corticosteroids in wild horse stallion. Comparative Biochemistry and Physiology a-Physiology 1977;57(1):179–81.
  63. Johnson AL, Malinowski K. Daily rhythm of cortisol, and evidence for a photo-inducible phase for prolactin secretion in nonpregnant mares housed under noninterrupted and skeleton photoperiods. Journal of Animal Science 1986;63(1):169–75.
    pubmed: 3733571
  64. Irvine CHG, Alexander SL. Factors affecting the circadian rhythm in plasma cortisol concentration in the horse. Domest Anim Endocrinol 1999;11:227–38.
    pubmed: 8045104
  65. Palme R, Fischer P, Schildorfer H, Ismail MN. Excretion of infused C-14-steroid hormones via faeces and urine in domestic livestock. Animal Reproduction Science 1996;43:43–63.
  66. Rochais C, Fureix C, Lesimple C, Hausberger M. Lower attention to daily environment: a novel cue for detecting chronic horses' back pain?. Scientific reports 2016;6:20117.
    doi: 10.1038/srep20117pmc: PMC4731760pubmed: 26823123google scholar: lookup
  67. Henry S, Fureix C, Rowberry R, Bateson M, Hausberger M. Do horses with poor welfare show 'pessimistic' cognitive biases?. Die Naturwissenschaften 2017;104(1–2):8.
    doi: 10.1007/s00114-016-1429-1pubmed: 28083632google scholar: lookup
  68. Ashley FH, Waterman-Pearson AE, Whay HR. Behavioural assessment of pain in horses and donkeys: application to clinical practice and future studies. Equine veterinary journal 2005;37.
    pubmed: 16295937
  69. Waring G. Horse Behavior, 2nd Edition Norwich, New York: Noyes Publications/WilliamAndrew Publishing. 2003.
  70. Reefmann N, Kaszas FB, Wechsler B, Gygax L. Ear and tail postures as indicators of emotional valence in sheep. Applied Animal Behaviour Science 2009;118(3–4):199–207.
    doi: 10.1016/j.applanim.2009.02.013google scholar: lookup
  71. Hausberger M, Muller C. A brief note on some possible factors involved in the reactions of horses to humans. Applied Animal Behaviour Science 2002;76(4):339–44.
  72. Haussler KK. Application of chiropractic principles and techniques to equine practice. Proc Ann Conv Am Assoc Equine Pract 1997. p. 312–8.
  73. Brauner S. Why Treating Animals and is there a Placebo Effect in the Treatment of Animals?. Chiropractic, A Vital Science (European Chiropractors' Union congress), Alghero, Sardinia, Italy 2009.
  74. Wood TG, Colloca CJ, Matthews R. A pilot randomized clinical trial on the relative effect of instrumental (MFMA) versus manual (HVLA) manipulation in the treatment of cervical spine dysfunction. Journal of Manipulative and Physiological Therapeutics 2001;24(4):260–71.
    doi: 10.1067/mmt.2001.114365pubmed: 11353937google scholar: lookup
  75. Shearar KA, Colloca CJ, White HL. A randomized clinical trial of manual versus mechanical force manipulation in the treatment of sacroiliac joint syndrome. Journal of Manipulative and Physiological Therapeutics 2005;28(7):493–501.
    doi: 10.1016/j.jmpt.2005.07.006pubmed: 16182023google scholar: lookup
  76. Cauvin E. Assessment of back pain in houses. Equine practice 1997;19(10):522–33.
  77. Gillis C. Spinal ligament pathology. Veterinary Clinics of North America-Equine Practice 1999;15(1):97–101.
    pubmed: 10218244
  78. Kirkaldy-Willis WH, Cassidy JD. Spinal Manipulation in the Treatment of Low-Back Pain. Canadian Familial Physician 1985;31:535–40.
    pmc: PMC2327983pubmed: 21274223
  79. Sullivan KA, Hill AE, Haussler KK. The effects of chiropractic, massage and phenylbutazone on spinal mechanical nociceptive thresholds in horses without clinical signs. Equine Veterinary Journal 2008;40(1):14–20.
    doi: 10.2746/042516407X240456pubmed: 18083655google scholar: lookup
  80. Jeffcott LB, Holmes MA, Townsend HGG. Validity of saddle pressure measurements using force-sensing array technology—Preliminary studies. Veterinary Journal 1999;158(2):113–9.
    pubmed: 10489267
  81. Landman M, de Blaauw JA, van Weeren PR, Hofland LJ. Field study of the prevalence of lameness in horses with back problems. Veterinary Record 2004;155(6):165–8.
    pubmed: 15357376
  82. McGreevy P, McLean A. Behavioural problems with the ridden horse. The Domestic Horse, The Origins, Development and Management of its Behaviour 2005. p. 196–211.
  83. Irvine CH, Alexander SL. Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domest Anim Endocrinol 1994;11(2):227–38.
    pubmed: 8045104
  84. Nogueira GP, Barnabe RC. Is the thoroughbred race-horse under chronic stress?. Braz J Med Biol Res 1997;30(10):1237–9.
    pubmed: 9496444
  85. Pruessner JC, Hellhammer DH, Kirschbaum C. Burnout, perceived stress, and cortisol responses to awakening. Psychosom Med 1999;61(2):197–204.
    pubmed: 10204973
  86. Ley SJ, Livingston A, Waterman AE. Effects of chronic lameness on the concentrations of cortisol, prolactin and vasopressin in the plasma of sheep. Veterinary Record 1991;129(3):45–7.
    pubmed: 1926698
  87. Juster RP, Sindi S, Marin MF, Perna A, Hashemi A, Pruessner JC. A clinical allostatic load index is associated with burnout symptoms and hypocortisolemic profiles in healthy workers. Psychoneuroendocrinology 2011;36(6):797–805.
    doi: 10.1016/j.psyneuen.2010.11.001pubmed: 21129851google scholar: lookup
  88. Muhtz C, Rodriguez-Raecke R, Hinkelmann K, Moeller-Bertram T, Kiefer F, Wiedemann K. Cortisol response to experimental pain in patients with chronic low back pain and patients with major depression. Pain Med 2013;14(4):498–503.
    doi: 10.1111/j.1526-4637.2012.01514.xpubmed: 23137117google scholar: lookup
  89. Selye H. The stress of life. New York: McGraw-Hill; 1956.
  90. McEwen BS. Mood disorders and allostatic load. Biological Psychiatry 2003;54(3):200–7.
    doi: 10.1016/s0006-3223(03)00177-xpubmed: 12893096google scholar: lookup
  91. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Hormones and Behavior 2003;43(1):2–15.
    doi: 10.1016/s0018-506x(02)00024-7pubmed: 12614627google scholar: lookup
  92. Korte SM, Olivier B, Koolhaas JM. A new animal welfare concept based on allostasis. Physiology & Behavior 2007;92(3):422–8.
    doi: 10.1016/j.physbeh.2006.10.018pubmed: 17174361google scholar: lookup
  93. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H. Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 1999;23(7):925–35.
    pubmed: 10580307
  94. Benhajali H, Richard-Yris MA, Leroux M, Ezzaouia M, Charfi F, Hausberger M. A note on the time budget and social behaviour of densely housed horses—A case study in Arab breeding mares. Applied Animal Behaviour Science 2008;112(1–2):196–200.
    doi: 10.1016/j.applanim.2007.08.007google scholar: lookup
  95. Benhajali H, Richard-Yris MA, Ezzaouia M, Charfi F, Hausberger M. Foraging opportunity: a crucial criterion for horse welfare?. Animal 2009;3(9):1308–12.
    doi: 10.1017/S1751731109004820pubmed: 22444907google scholar: lookup
  96. Mateo JM. Inverted-U shape relationship between cortisol and learning in ground squirrels. Neurobiology of Learning and Memory 2008;89(4):582–90.
    doi: 10.1016/j.nlm.2007.11.002pmc: PMC2435239pubmed: 18164635google scholar: lookup
  97. Parker M, Redhead ES, Goodwin D, McBride SD. Impaired instrumental choice in crib-biting horses (Equus caballus). Behav Brain Res 2008;191(1):137–40.
    doi: 10.1016/j.bbr.2008.03.009pubmed: 18430476google scholar: lookup
  98. Rochais C, Henry S, Fureix C, Hausberger M. Investigating attentional processes in depressive-like domestic horses (Equus caballus). Behavioural processes 2016;124:93–6.
    doi: 10.1016/j.beproc.2015.12.010pubmed: 26739514google scholar: lookup
  99. Mostl E, Palme R. Hormones as indicators of stress. Domest Anim Endocrinol 2002;23(1–2):67–74.
    pubmed: 12142227
  100. Pell SM, McGreevy PD. A study of cortisol and beta-endorphin levels in stereotypic and normal Thoroughbreds. Applied Animal Behaviour Science 1999;64(2):81–90.
  101. Lebelt D, Schonreiter S, Zanella AJ. Salivary cortisol in stallions: The relationship with plasma levels, daytime profile and changes in response to semen collection. Pferdeheilkunde 1996;12(4):411–4.
  102. Siiteri PK, Murai JT, Hammond GL, Nisker JA, Raymoure WJ, Kuhn RW. The serum transport of steroid hormones. Recent Prog Horm Res 1982;38:457–510.
    pubmed: 6750727
  103. Bae YJ, Kratzsch J. Corticosteroid-binding globulin: modulating mechanisms of bioavailability of cortisol and its clinical implications. Best Pract Res Clin Endocrinol Metab 2015;29(5):761–72.
    doi: 10.1016/j.beem.2015.09.001pubmed: 26522460google scholar: lookup
  104. Mostl E, Messmann S, Bagu E, Robia C, Palme R. Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Journal of Veterinary Medicine Series a-Physiology Pathology Clinical Medicine 1999;46(10):621–31.
    pubmed: 10638300
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.