Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T09:09:48.847Z Has data issue: false hasContentIssue false

Evaluation of the effect of tongue ties on stress parameters, behaviour and heart-rate variability in racehorses

Published online by Cambridge University Press:  01 January 2023

A Barton*
Affiliation:
Equine Clinic, Freie Universitaet Berlin, Oertzenweg 19b, 14163 Berlin, Germany
I Lindenberg
Affiliation:
Equine Clinic, Freie Universitaet Berlin, Oertzenweg 19b, 14163 Berlin, Germany
A Einspanier
Affiliation:
Institute of Veterinary Physiological Chemistry, An den Tierkliniken 7/7a, University Leipzig, 04103 Leipzig, Germany
R Merle
Affiliation:
Institute of Veterinary Epidemiology, Freie Universitaet Berlin, Oertzenweg 19b, 14163 Berlin, Germany
H Gehlen
Affiliation:
Equine Clinic, Freie Universitaet Berlin, Oertzenweg 19b, 14163 Berlin, Germany
*
* Contact for correspondence: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Fixation of the tongue to the mandible using so-called tongue ties (TTs) is common practice in Standardbred (SB) and Thoroughbred (TB) racing, but little is known about their impact on animal welfare. In this study, the influence of TTs on heart-rate variability (HRV), stress parameters in plasma (cortisol, glucose, lactate) and behaviour was evaluated in 30 SBs and 29 TBs (n = 59) presenting with exercise insufficiency. Overall, 36/59 horses (24 SBs, 12 TBs) were familiar with TTs. Blood was taken at rest, after TT application and after racing in all horses, additionally samples were taken without TT in SBs another day. HRV was calculated over 3 min before, during and after racing. Additionally, SBs’ behaviour during TT application and racing was documented in real time. TT application did not increase cortisol levels significantly, while highly significant increases in cortisol levels were found after racing. Lactate levels were not influenced by TT application, but also significantly increased after racing. No significant differences were found for glucose. Seventeen out of 30 SBs showed mild (n = 8), moderate (n = 8) and severe (n = 1) reactions during TT application, none during or after race training. At rest, 23/30 SBs had a low/high frequency (LF/HF) ratio < 1.5 (1.05 [± 0.61], n = 30, dominating parasympathetic activity). After TT application, the LF/HF ratio increased to 1.4 (± 0.45) (increased sympathetic activity). In TBs, sympathetic activity dominated at rest. No differences in LF, HF and LF/HF were found after TT application or comparing HRV after racing with/without TT. The stress response (blood parameters and HRV) was not influenced by horses’ naivety to TTs, however an increased stress response was observed in SB mares. Overall, obvious adverse behaviour, but only slight evidence of an increased systemic stress response, was found in this study. These results might provide objective evidence for future decisions from equine sports organisations concerning further regulations on TTs.

Type
Research Article
Copyright
© 2022 Universities Federation for Animal Welfare

References

Alexander, SL and Irvine, CH 1998 The effect of social stress on adrenal axis activity in horses: the importance of monitoring corticosteroid-binding globulin capacity. The Journal of Endocrinology 157: 425432. https://doi.org/10.1677/joe.0.1570425CrossRefGoogle ScholarPubMed
Alexander, SL, Irvine, CH and Donald, RA 1996 Dynamics of the regulation of the hypothalamo-pituitary-adrenal (HPA) axis determined using a nonsurgical method for collecting pituitary venous blood from horses. Frontiers in Neuroendocrinology 17: 150. https://doi.org/10.1006/frne.1996.0001CrossRefGoogle ScholarPubMed
Bachmann, I, Bernasconi, P, Herrmann, R, Weishaupt, MA and Stauffacher, M 2003 Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Applied Animal Behaviour Science 82: 297311. https://doi.org/10.1016/S0168-1591(03)00086-8CrossRefGoogle Scholar
Barakzai, SZ and Dixon, PM 2005 Conservative treatment for thoroughbred racehorses with intermittent dorsal displacement of the soft palate. The Veterinary Record 157: 337340. https://doi.org/10.1136/vr.157.12.337CrossRefGoogle ScholarPubMed
Barakzai, SZ, Finnegan, C and Boden, LA 2009a Effect of ‘tongue tie’ use on racing performance of thoroughbreds in the United Kingdom. Equine Veterinary Journal 41: 812816. https://doi.org/10.2746/042516409X434134CrossRefGoogle ScholarPubMed
Barakzai, SZ, Finnegan, C, Dixon, PM, Hillyer, MH and Boden, LA 2009b Use of tongue ties in thoroughbred racehorses in the United Kingdom, and its association with surgery for dorsal displacement of the soft palate. The Veterinary Record 165: 278281. https://doi.org/10.1136/vr.165.10.278CrossRefGoogle ScholarPubMed
Barton, A, Lindenberg, I, Klaus, D, Blohm, KO and Gehlen, H 2019 Casuistic evaluation of tongue tie use in Standardbred and Thoroughbred racehorses in Germany – a questionnaire study. Equine Medicine 35: 17. https://doi.org/10.21836/PEM20190503CrossRefGoogle Scholar
Becker-Birck, M, Schmidt, A, Wulf, M, Aurich, J, von der Wense, A, Möstl, E, Berz, R and Aurich, C 2013 Cortisol release, heart rate and heart rate variability, and superficial body temperature, in horses lunged either with hyperflexion of the neck or with an extended head and neck position. Journal of Animal Physiology and Animal Nutrition 97: 322330. https://doi.org/10.1111/j.1439-0396.2012.01274.xCrossRefGoogle ScholarPubMed
Berntson, GG, Bigger, JT, Eckberg, DL, Grossmann, P, Kaufmann, PG, Malik, M, Nagaraja, HN, Porges, SW, Saul, JP, Stone, PH and van der Molen, MW 1997 Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology 34: 623648. https://doi.org/10.1111/j.1469-8986.1997.tb02140.xCrossRefGoogle ScholarPubMed
Bertin, FR, Taylor, SD, Bianco, AW and Sojka-Kritchevsky, JE 2016 The effect of fasting duration on baseline blood glucose concen-tration, blood insulin concentration, glucose/insulin ratio, oral sugar test, and insulin response test results in horses. Journal of Veterinary Internal Medicine 30: 17261731. https://doi.org/10.1111/jvim.14529CrossRefGoogle Scholar
Brüggemann, T 1995 Spektralanalyse zur Beurteilung der Herzfrequenzvariabilität. Herzschrittmachertherapie & Elektrophysiologie 5: 1924. [Title translation: Spectral analysis for evaluation of heart rate variability]Google Scholar
Cayado, P, Munoz-Escassi, B, Dominguez, C, Manley, W, Olabarri, B, Sanchez de la Muela, M, Castejon, F, Maranon, G and Vara, E 2006 Hormone response to training and competition in athletic horses. Equine Veterinary Journal Supplements 36: 274278. https://doi.org/10.1111/j.2042-3306.2006.tb05552.xCrossRefGoogle Scholar
Chalmers, HJ, Farberman, A, Bermingham, A, Sears, W and Viel, L 2013 The use of a tongue tie alters laryngohyoid position in the standing horse. Equine Veterinary Journal 45: 711714. https://doi.org/10.1111/evj.12056CrossRefGoogle ScholarPubMed
Cottin, F, Barrey, E, Lopes, P and Billat, V 2006 Effect of repeat-ed exercise and recovery on heart rate variability in elite trotting horses during high intensity interval training. Equine Veterinary Journal Supplements 38: 204209. https://doi.org/10.1111/j.2042-3306.2006.tb05540.xCrossRefGoogle Scholar
Cottin, F, Medique, C, Lopes, P, Petit, E, Papelier, Y and Billat, VL 2005 Effect of exercise intensity and repetition on heart rate variability during training in elite trotting horse. International Journal of Sports Medicine 26: 859867. https://doi.org/10.1055/s-2005-837462CrossRefGoogle ScholarPubMed
Cravana, C, Medica, P, Prestopino, M, Fazio, E and Ferlazzo, A 2010 Effects of competitive and noncompetitive showjumping on total and free iodothyronines, beta-endorphin, ACTH and cor-tisol levels of horses. Equine Veterinary Journal Supplements 38: 179184. https://doi.org/10.1111/j.2042-3306.2010.00264.xCrossRefGoogle Scholar
Direktorium für Vollblutzucht und Rennen eV 2018 Der Einsatz von Zungenbändern ist ab 1 Juni verboten. Pressemeldung. https://www.german-racing.com/gr/aktuelles/meldungen/20180531-310518-news-zunge.php. [Title translation: Use of tongue ties is for-bidden from June 1st]Google Scholar
Eckberg, DL 1997 Sympathovagal balance: a critical appraisal. Circulation 96: 32243232. https://doi.org/10.1161/01.CIR.96.9.3224CrossRefGoogle ScholarPubMed
Evans, JW 1971 Effect of fasting, gestation, lactation and exercise on glucose turnover in horses. Journal of Animal Science 33: 10011004. https://doi.org/10.2527/jas1971.3351001xCrossRefGoogle ScholarPubMed
Fazio, E, Medica, P, Aronica, V, Grasso, L and Ferlazzo, A 2008 Circulating beta-endorphin, adrenocorticotrophic hormone and cortisol levels of stallions before and after short road transport: stress effect of different distances. Acta Veterinaria Scandinavica 50: 6. https://doi.org/10.1186/1751-0147-50-6CrossRefGoogle ScholarPubMed
Fazio, E, Medica, P, Cravana, C and Ferlazzo, A 2013 Cortisol response to road transport stress in calm in and nervous stallions. Journal of Veterinary Behaviour 8: 231237. https://doi.org/10.1016/j.jveb.2012.10.010CrossRefGoogle Scholar
Fenner, K, Yoon, S, White, P, Starling, M and McGreevy, P 2016 The effect of noseband tightening on horses’ behavior, eye temperature, and cardiac responses. PLoS One 11(5): e0154179. https://doi.org/10.1371/journal.pone.0154179CrossRefGoogle ScholarPubMed
Ferlazzo, A, Medica, P, Cravana, C and Fazio, E 2009 Endocrine changes after experimental showjumping. Comparative Exercise Physiology 6: 5966. https://doi.org/10.1017/S1755254009990110CrossRefGoogle Scholar
Findley, JA, Sealy, H and Franklin, SH 2016 Factors associated with tongue tie use in Australian Standardbred racehorses. Equine Veterinary Journal 48: 530. https://doi.org/10.1111/evj.32_12612Google Scholar
Golland, LC, Evans, DL, Stone, GM, Tyler-McGowan, CM, Hodgson, DR and Rose, RJ 1999 Plasma cortisol and beta-endorphin concentrations in trained and over-trained standard-bred racehorses. Pflugers Archiv: European Journal of Physiology 439: 1117. https://doi.org/10.1007/s004249900111Google Scholar
Harbuz, MS and Lightman, SL 1992 Stress and the hypothala-mo-pituitary-adrenal axis: acute, chronic and immunological activation. Journal of Endocrinology 134(3): 327339. https://doi.org/10.1677/joe.0.1340327CrossRefGoogle ScholarPubMed
Harris, P and Snow, DH 1988 The effects of high intensity exer-cise on the plasma concentration of lactate, potassium and other electrolytes. Equine Veterinary Journal 20: 109113. https://doi.org/10.1111/j.2042-3306.1988.tb01470.xCrossRefGoogle Scholar
Hodgson, DR, Kelso, IB, Bayly, WM and Gollnick, PD 1987 Responses to repeated high intensity exercise: influence on muscle metabolism. Equine Veterinary Journal 302-311Google Scholar
Hoffsis, GF and Murdick, PW 1970b The plasma concentrations of corticosteroids in normal and diseased horses. Journal of the American Veterinary Medical Association 157: 15901594Google ScholarPubMed
Hoffsis, GF, Murdick, PW, Tharp, VL and Ault, K 1970a Plasma concentrations of cortisol and corticosterone in the normal horse. American Journal of Veterinary Research 31: 13791387Google ScholarPubMed
Horohov, DW, Dimock, A, Guirnalda, P, Folsom, RW, McKeever, KH and Malinowski, K 1999 Effect of exercise on the immune response of young and old horses. American Journal of Veterinary Research 60: 643647. https://doi.org/10.21836/PEM19960410Google Scholar
Hottenrott, K 2002 Grundlagen zur Herzfrequenzvariabilität und Anwendungs-möglichkeiten im Sport. Herzfrequenzvariabilität im Sport - Prevention, Rehabilitation and Training. K Czwalina Verlag: Hottenrott Hamburg, Germany. [Title translation: Basics of heart rate variability and applications in sports medicine. Heart rate variability in sports - prevention, rehabilitation and training]Google Scholar
Houle, MS and Billman, GE 1999 Low-frequency component of the heart rate variability spectrum: a poor marker of sympathetic activity. American Journal of Physiology 276: 215223. https://doi.org/10.1152/ajpheart.1999.276.1.H215Google ScholarPubMed
Hydbring, E, Nyman, S and Dahlborn, K 1996 Changes in plas-ma cortisol, plasma beta-endorphin, heart rate, haematocrit and plasma protein concentration in horses during restraint and use of naso-gastric tube. Equine Medicine 12: 423427.CrossRefGoogle Scholar
Kindermann, W, Simon, G and Keul, J 1979 The significance of the aerobic-anaerobic transition for the determination of work load intensities during endurance training. European Journal of Applied Physiology and Occupied Physiology 42: 2534. https://doi.org/10.1007/BF00421101CrossRefGoogle ScholarPubMed
Krzywanek, H, Schulze, A and Wittke, G 1972 Behavior of var-ious blood parameters in trotters following defined exertion. Berliner und Münchener Tierärztliche Wochenschrift 85: 325329Google Scholar
Kucera, M 2006 Herzfrequenzvariabilität. 36001 Karlovy Vary: Czech Republic. [Title translation: Heart rate variability]Google Scholar
Kuwahara, M, Hashimoto, S, Ishii, K, Yagi, Y, Hada, T, Hiraga, A, Kai, M, Kubo, K, Oki, H, Tsubone, H and Sugano, S 1996 Assessment of autonomic nervous function by power spectral analysis of heart rate variability in the horse. Journal of the Autonomic Nervous System 60: 4348. https://doi.org/10.1016/0165-1838(96)00028-8CrossRefGoogle ScholarPubMed
Kuwahara, M, Hiraga, A, Kai, M, Tsubone, H and Sugano, S 1999 Influence of training on autonomic nervous function in hors-es: evaluation by power spectral analysis of heart rate variability. Equine Veterinary Journal Supplements 30: 178180. https://doi.org/10.1111/j.2042-3306.1999.tb05213.xGoogle Scholar
Latimer-Marsh, L, Hazel, S, Santos, L and McGreevy, PD 2017 The effect of tongue-tie application on stress responses in resting horses. World Equine Airways Symposium. 13-15 July 2017, Copenhagen, DenmarkGoogle Scholar
Lindner, A, von Wittke, P, Schmald, M, Kusserov, J and Sommer, H 1992 Maximal lactate concentrations in horses after exercise of different duration and intensity. Journal of Equine Veterinary Science 12: 3033. https://doi.org/10.1016/S0737-0806(06)81384-5CrossRefGoogle Scholar
Luna, SP, Taylor, PM and Wheeler, MJ 1996 Cardiorespiratory, endocrine and metabolic changes in ponies undergoing intra-venous or inhalation anaesthesia. Journal of Veterinary Pharmacology and Therapeutics 19: 251258. https://doi.org/10.1111/j.1365-2885.1996.tb00046.xCrossRefGoogle ScholarPubMed
Malik, MD 1996 Heart rate variability. Standards of measurement, physiological interpretation, and clinical use: Task Force of the European Society of Cardiology and the North American Society for Pacing and Electrophysiology. European Heart Journal 17: 354381CrossRefGoogle Scholar
Malinowski, K, Shock, EJ, Rochelle, P, Kearns, CF, Guirnalda, PD and McKeever, KH 2006 Plasma beta-endorphin, cortisol and immune responses to acute exercise are altered by age and exercise training in horses. Equine Veterinary Journal Supplements 30: 267273. https://doi.org/10.1111/j.2042-3306.2006.tb05551.xCrossRefGoogle Scholar
Malliani, A, Pagani, M, Lombardi, F and Cerutti, F 1991 Cardiovascular neural regulation explored in the frequency domain. Circulation 84(2): 482492. https://doi.org/10.1161/01.CIR.84.2.482CrossRefGoogle ScholarPubMed
Martínez, R, Godoy, A, Naretto, E and White, A 1988 Neuroendocrine changes produced by competition stress on the Thoroughbred race horse. Comparative Biochemistry and Physiology: A Comparative Physiology 91: 599602. https://doi.org/10.1016/0300-9629(88)90640-8CrossRefGoogle ScholarPubMed
May, A 2007 Evaluierung von Stressparametern beim Pferd im Zusammenhang mit dem Klinikaufenthalt. Doctoral Thesis, Veterinary Faculty of Ludwig-Maximilian-University Munich, Germany. [Title translation: Evaluation of stress parameters in horses during hospital stay]Google Scholar
Medica, P, Bruschetta, G, Cravana, C, Ferlazzo, A and Fazio, E 2019 Effect of transportation on the sympatho-adrenal system responses in horses Research in Veterinary Science 125: 401404. https://doi.org/10.1016/j.rvsc.2017.10.001CrossRefGoogle ScholarPubMed
Medica, P, Cravana, C, Fazio, E and Ferlazzo, A 2011 24 hour endocrine profiles of quarter horses under resting conditions Equine Veterinary Science 31: 3540. https://doi.org/10.1016/j.jevs.2010.11.015CrossRefGoogle Scholar
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 6774. https://doi.org/10.1016/S0739-7240(02)00146-7CrossRefGoogle ScholarPubMed
Ohmura, H, Hiraga, A, Aida, H, Kuwahara, M and Tsubone, H 2002 Effects of initial handling and training on autonomic nervous function in young Thoroughbreds. American Journal of Veterinary Research 63: 14881491. https://doi.org/10.2460/ajvr.2002.63.1488CrossRefGoogle ScholarPubMed
Ohmura, H, Hobo, S, Hiraga, A and Jones, JH 2012 Changes in heart rate and heart rate variability during transportation of hors-es by road and air. American Journal of Veterinary Research 73: 515521. https://doi.org/10.2460/ajvr.73.4.515CrossRefGoogle ScholarPubMed
Pagani, M, Lombardi, F, Guzzetti, S, Rimoldi, O, Furlan, R, Pizzinelli, P, Sandrone, G, Malfatto, G, Dell’Orto, S and Piccaluga, E 1986 Power spectral analysis of heart rate and arte-rial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circulation Research 59: 178193. https://doi.org/10.1161/01.RES.59.2.178CrossRefGoogle Scholar
Physick-Sheard, PW, Marlin, DJ, Thornhill, R and Schroter, RC 2000 Frequency domain analysis of heart rate variability in horses at rest and during exercise. Equine Veterinary Journal 32: 253262. https://doi.org/10.2746/042516400776563572CrossRefGoogle ScholarPubMed
Pomeranz, B, Macaulay, RJ, Caudill, MA, Kutz, I, Adam, D, Gordon, D, Kilborn, KM, Barger, AC, Shannon, DC and Cohen, RJ 1985 Assessment of autonomic function in humans by heart rate spectral analysis. American Journal of Physiology 248: 151153. https://doi.org/10.1152/ajpheart.1985.248.1.H151Google ScholarPubMed
Quick, JS and Warren-Smith, AK 2009 Preliminary investigations of horses’ (Equus caballus) responses to different bridles during foundation training. Journal of Veterinary Behaviour 4: 169176. https://doi.org/10.1016/j.jveb.2008.12.001CrossRefGoogle Scholar
Rainger, JE, Evans, DL, Hodgson, DR and Rose, RJ 1994 Blood lactate disappearance after maximal exercise in trained and detrained horses. Research in Veterinary Science 57: 325331. https://doi.org/10.1016/0034-5288(94)90125-2CrossRefGoogle ScholarPubMed
Ralston, SL 2002 Insulin and glucose regulation. The Veterinary Clinics of North America: Equine Practice 18: 295304. https://doi.org/10.1016/S0749-0739(02)00014-7.Google ScholarPubMed
Roberts, CA, Marlin, DJ and Lekeux, P 1999 The effects of training on ventilation and blood gases in exercising thorough-breds. Equine Veterinary Journal Supplements 30: 5761. https://doi.org/10.1111/j.2042-3306.1999.tb05189.xGoogle Scholar
Rompelman, O, Coenen, AJ and Kitney, RI 1977 Measurement of heart-rate variability: Part 1-Comparative study of heart-rate variability analysis methods. Medical and Biological Engineering and Computing 15: 233239. https://doi.org/10.1007/BF02441043CrossRefGoogle ScholarPubMed
Rose, RJ, Hodgson, DR, Kelso, TB, McCutcheon, LJ, Reid, TA, Bayly, WM and Gollnick, PD 1988 Maximum O2 uptake, O2 debt and deficit, and muscle metabolites in Thoroughbred horses. Journal of Applied Physiology 64: 781788. https://doi.org/10.1152/jappl.1988.64.2.781CrossRefGoogle ScholarPubMed
Sammito, S and Bockelmann, I 2015 Analysis of heart rate variability. Mathematical description and practical application. Herz 40 Suppl 1: 7684. https://doi.org/10.1007/s00059-014-4145-7CrossRefGoogle Scholar
Schmidt, A, Aurich, J, Möstl, E, Müller, J and Aurich, C 2010a Changes in cortisol release and heart rate and heart rate variability during the initial training of 3-year-old sport horses. Hormones and Behaviour 58: 628636. https://doi.org/10.1016/j.yhbeh.2010.06.011CrossRefGoogle ScholarPubMed
Schmidt, A, Biau, S, Möstl, E, Becker-Birck, M, Morillon, B, Aurich, J, Faure, JM and Aurich, C 2010b Changes in cortisol release and heart rate variability in sport horses during long-distance road transport. Domestic Animal Endocrinology 38: 179189. https://doi.org/10.1016/j.domaniend.2009.10.002CrossRefGoogle ScholarPubMed
Schmidt, A, Hödl, S, Möstl, E, Aurich, J, Müller, J and Aurich, C 2010c Cortisol release, heart rate, and heart rate variability in transport-naive horses during repeated road transport. Domestic Animal Endocrinology 39: 205213. https://doi.org/10.1016/j.doma-niend.2010.06.002CrossRefGoogle ScholarPubMed
Schmidt, A, Möstl, E, Wehnert, C, Aurich, J, Müller, J and Aurich, C 2010d Cortisol release and heart rate variability in horses during road transport. Hormones and Behaviour 57: 209215. https://doi.org/10.1016/j.yhbeh.2009.11.003CrossRefGoogle ScholarPubMed
Stull, CL and Rodiek, AV 2002 Effects of cross-tying horses during 24 h of road transport. Equine Veterinary Journal 34: 550555. https://doi.org/10.2746/042516402776180214CrossRefGoogle ScholarPubMed
Tarvainen, MP, Niskanen, JP, Lipponen, JA, Ranta-Aho, PO and Karjalainen, PA 2014 Kubios HRV-heart rate variability analysis software. Computer Methods and Programs in Biomedicine 113: 210220. https://doi.org/10.1016/j.cmpb.2013.07.024CrossRefGoogle ScholarPubMed
Thayer, JF, Hahn, AW, Pearson, MA, Sollers JJ, III, Johnson, PJ and Loch, WE 1997 Heart rate variability during exercise in the horse. Biomedical Sciences Instrumentation 34: 246251Google ScholarPubMed
van Breda, E 2006 A nonnatural head-neck position (Rollkur) during training results in less acute stress in elite, trained, dressage horses. Journal of Applied Animal Welfare Science 9: 5964. https://doi.org/10.1207/s15327604jaws0901_5CrossRefGoogle ScholarPubMed
Vervuert, I 2011 Fütterungsempfehlungen bei Muskelerkrankungen des Pferdes: Stand der Forschung versus Supplementiasis. Der Praktische Tierarzt 11: 988992. [Title translation: The vet in practice]Google Scholar
Visser, EK, van Reenen, CG, van der Werf, JTN, Schilder, MBH, Knaap, JH, Barneveld, A and Blokhuis, HJ 2002 Heart rate and heart rate variability during a novel object test and a han-dling test in young horses. Physiology and Behaviour 76: 289296. https://doi.org/10.1016/S0031-9384(02)00698-4CrossRefGoogle Scholar
Wagner, AE 2010 Effects of stress on pain in horses and incorporating pain scales for equine practice. The Veterinary Clinics of North America: Equine Practice 26: 481492. https://doi.org/10.1016/j.cveq.2010.07.001Google ScholarPubMed
Walther, M 2017 Untersuchung zur Tötung von Pferden. Doctoral Thesis, Veterinary Department, Freie Universitaet Berlin, Germany. [Title translation: Evaluation on the euthanasia of horses]Google Scholar
Zebisch, A, May, A, Reese, S and Gehlen, H 2014 Effect of dif-ferent head-neck positions on physical and psychological stress parameters in the ridden horse. Journal of Animal Physiology and Animal Nutrition 98: 901907. https://doi.org/10.1111/jpn.12155CrossRefGoogle Scholar