Heart rate variability and saliva cortisol assessment in shelter dog: Human-animal interaction effects

Applied Animal Behaviour Science

Volumn 125, Issue 1-2, 2010, Pages 56-68

  Bergamasco, Luciana ^a   Osella, Maria Cristina ^b   Savarino, Paolo ^c   Larosa, Giuseppe ^d   Ozella, Laura ^e   Manassero, Monica ^f   Badino, Paola ^c   Odore, Rosangela ^c   Barbero, Raffaella ^c   Re, Giovanni ^c  

^a Analytical and Toxicological Services   (United States)

^b Pherosyntheses Research Institute Semiochemistry and Applied Ethology   (France)

^c UNIVERSITY OF TURIN   (Italy)

^d Borio Veterinary Clinic   (Italy)

^e Sempione Veterinary Clinic   (Italy)

^f Ottino and Picatti Veterinary Clinic   (Italy)

Author keywords

Cortisol; Heart rate variability; Human dog interactions; Shelter dogs; Stress; Welfare

Indexed keywords

ANIMAL WELFARE; BEHAVIORAL ECOLOGY; CANID; CARDIOLOGY; CARDIOVASCULAR SYSTEM; HORMONE; PHYSIOLOGY; SALIVA; SHELTER;

ANIMALIA; CANIS FAMILIARIS;

EID: 77953326843     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2010.03.002     Document Type: Article

References (74)

1. Akselrod S. Components of heart rate variability: basic studies. In: Malik M., and Camm A.J. (Eds). Heart Rate Variability (1995), Futura Publishing Company Inc., Armonk N.Y. 147-163
2. Bachmann I., Bernasconi P., Hermann R., Weishaupt M.A., and Stauffacher M. Behavioural and physiological responses to an acute stressor in cribbiting and control horses. Appl. Anim. Behav. Sci. 82 (2003) 297-311
3. Beauchaine T. Vagal tone, development, and Gray's motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology. Dev. Psychopathol. 13 (2001) 183-214
4. Beerda B., Schilder M.B.H., Janssen N.S.C.R.M., and Mol A.J. The use of saliva cortisol, urinary cortisol and catecholamine measurements for a noninvasive assessment of stress response in dogs. Horm. Behav. 30 (1996) 272-279
5. Beerda B., Schilder M.B.H., van Hooff J.A.R.A.M., de Vries H.W., and Mol J.A. Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Appl. Anim. Behav. Sci. 58 (1998) 365-381
6. Beerda B., Schilder M.B.H., Bernardina W., Van Hoof J.A.R.A.M., De Vries H.W., and Mol J.A. Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiol. Behav. 66 (1999) 243-254
7. Boxall J., Heath S., Bate S., and Brautigam J. Modern concepts of socialization for dogs: implications for their behaviour, welfare and use in scientific procedures. Altern. Lab. Anim. 32 Suppl. 2 (2004) 81-93
8. Cacioppo J., Malaarkey W., Kiecolt-Glaser J., Uchino B., Sgoutas-Emch S., Sheridan J., Berntson G., and Glaser R. Heterogeneity in neuroendocrine and immune responses to brief psychological stressors as a function of autonomic cardiac activation. Psychosom. Med. 57 (1995) 154-164
9. Calvert C.A., and Jacobs G.J. Heart rate variability in Doberman Pinschers with and without echocardiographic evidence of dilated cardiomyopathy. Am. J. Vet. Res. 65 (2000) 506-511
10. Calvert C.A., and Wall T.M. Correlations among time and frequency measures of heart rate variability recorded by use of Holter monitor in overtly healthy Doberman Pinschers with and without echocardiographic evidence of dilated cardiomyopathy. Am. J. Vet. Res. 62 (2001) 1787-1792
11. Colloca L., and Benedetti F. Placebos and painkillers: is mind as real as matter?. Nat. Rev. Neurosci. 6 (2005) 545-552
12. Cook N.J., Schaefer A.L., Lepage P., and Jones S.M. Salivary vs. serum cortisol for the assessment of adrenal activity in swine. Can. J. Anim. Sci. 76 (1996) 329-335
13. Cook N.J., Schaefer A.L., and Lepage P. Morgan Jones S.D. radioimmunoassay for cortisol in pig saliva and serum. J. Agric. Food Chem. 45 (1997) 395-399
14. Coppola C.L., Grandin T., and Enns R.M. Human interaction and cortisol: can contact reduce stress for shelter dogs?. Physiol. Behav. 87 (2006) 537-541
15. Désiré L., Veissier I., Desprès G., and Boissy A. On the way to assess emotions in animals: do lambs (Ovis aries) evaluate an event through its suddenness, novelty, or unpredictability?. J. Comp. Psychol. 118 (2004) 363-374
16. Diego M., Field T., and Hernandez-Reif M. Vagal activity, gastric motility, and weight gain massaged preterm neonates. J. Pediatrics 147 (2005) 50-55
17. Fox P.R., Sisson D., and Moise N.S. Textbook of Canine and Feline Cardiology: Principles and Clinical Practice. 2nd ed. (1999), WB Saunders, Philadelphia
18. Friedman B.H., and Thayer J.F. Autonomic balance revisited: panic anxiety and heart rate variability. J. Psychosom. Res. 44 (1998) 133-151
19. Geverink N.A., Schouten E.G., Gort G., and Wiegant V.M. Individual differences in behavioural and physiological responses to restraint stress in pigs. Physiol. Behav. 77 (2002) 451-457
20. Groschl M., Biskupek-Sigwart J., Rauh M., and Dorr H.G. Measurement of cortisol in saliva using a commercial radioimmunoassay developed for serum. J. Lab. Med. 24 (2000) 314-319
21. Gunnar M., Porter F., Wolf C., Rigatuso J., and Larson M. Neonatal stress reactivity: predictions to later emotional temperament. Child Dev. 66 (1995) 1-13
22. Hagen K., Langbein J., Schmied C., Lexer D., and Waiblinger S. Heart rate variability in dairy cows-influences of breed and milking system. Physiol. Behav. 85 (2005) 195-204
23. Hennessy M.B., Davis H.N., Williams M.T., Mellott C., and Douglas C.W. Plasma cortisol levels of dogs at a county animal shelter. Physiol. Behav. 62 (1997) 485-490
24. Hennessy M.B., Williams M.T., Miller D.D., Douglas C.W., and Voith V.L. Influence of male and female petters on plasma cortisol and behaviour: can human interaction reduce the stress of dogs in a public animal shelter?. Appl. Anim. Behav. Sci. 61 (1998) 63-77
25. Hennessy M.B., Voith V.L., Hawke J.L., Young T.L., Centrone J., McDowell A.L., Linden F., and Davenport G.M. Effects of a program of human interaction and alterations in diet composition on activity of the hypothalamic-pituitary-adrenal axis in dogs housed in a public animal shelter. J. Am. Vet. Med. Assoc. 221 (2002) 65-71
26. Herrnstein R.J. Placebo effect in the rat. Science 138 (1962) 677-678
27. Hubrecht R.H., and Turner D.C. Companion animal welfare in private and institutional settings. In: Wilson C.C., and Turner D.C. (Eds). Companion Animal in Human Health (1998), Sage Publications, Thousand Oaks, CA 267-289
28. Johansen O., Brox J., and Flaten M.A. Placebo and nocebo responses, cortisol, and circulating beta-endorphin. Psychosom. Med. 65 (2003) 786-790
29. Jones C.A., Refsal K.R., Lippert A.C., Nachreiner R.F., and Schwacha M.M. Changes in adrenal cortisol secretion as reflected in the urinary cortisol/creatinine ratio in dogs. Domest. Anim. Endocrinol. 7 (1990) 559-572
30. Kirschbaum C., and Hellhammer D.H. Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 22 (1989) 150-169
31. Kirschbaum C., and Hellhammer D.H. Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19 (1994) 313-333
32. Kobelt A.J., Hemsworth P.H., Barnett J.L., and Butler K.L. Sources of sampling variation in saliva cortisol in dogs. Res. Vet. Sci. 75 (2003) 157-161
33. Korte S.M., Ruesnik W., and Blokhuis H.J. Heart rate variability during manual restraint in chicks from high- and low-feather pecking lines of laying hens. Physiol. Behav. 65 (1999) 649-652
34. Kostarczyk E., and Fonberg E. Heart rate mechanisms in instrumental conditioning reinforced by petting in dogs. Physiol. Behav. 28 (1982) 27-30
35. Kraus M.S., Moise N.S., Rishniw M., Dykes N., and Erb H.N. Morphology of ventricular arrhythmias in the boxer as a measured by 12-lead electrocardiography with pace-mapping comparison. J. Vet. Int. Med. (2002) 153-158
36. Kuwahara M., Hiraga A., Kai M., Tsubone H., and Sugano S. Influence of training on autonomic nervous function in horses: evaluation by power spectral analysis of heart rate variability. Equine Vet. J. Suppl. 30 (1999) 178-180
37. Kuwahara M., Tsujino Y., Tsubone H., Kumagai E., Tsutsumi H., and Tanigawa M. Effects of pair housing on diurnal rhythms of heart rate and heart rate variability in miniature swine. Exp. Anim. (Tokyo) 53 (2004) 303-309
38. Ladewig J. Endocrine aspects of stress: evaluation of stress reactions in farm animals. In: Wiepkema P.R., and Adrichem P.W.M. (Eds). Biology of Stress in Farm Animals (1987), Martinus Nijhoff Publisher, Dordrecht 13-25
39. Langbein J., Nürnberg G., and Manteuffel G. Visual discrimination learning in dwarf goats and associated changes in heart rate and heart rate variability. Physiol. Behav. 82 (2004) 601-609
40. Legge 14 agosto 1991, n. 281: "Legge quadro in materia di animali di affezione e prevenzione del randagismo". Gazzetta Ufficiale della Repubblica Italiana del 30 agosto 1991.
41. Little C.J., Julu P.O., Hansen S., and Reid S.W. Real-time measurements of cardiac vagal tone in conscious dogs. Am. J. Physiol. 276 (1999) H758-H765
42. Lore R.K., and Eisenberg F.B. Avoidance reaction of domestic dogs to unfamiliar male and female humans in a kennel setting. Appl. Anim. Behav. Sci. 15 (1986) 262-266
43. Lucidi P., Barnabò N., Panunzi M., Dalla Villa P., and Mattioli M. Ethotest: a new model to identify (shelter) dogs' skills as service animals or adoptable pets. Appl. Anim. Behav. Sci 95 (2005) 103-122
44. Maros K., Dóka A., and Miklósi A. Behavioural correlation of heart rate changes in family dogs. Appl. Anim. Behav. Sci. 109 (2008) 329-341
45. McCraty R., Atkinson M., Tiller W.A., Rein G., and Watkins A.D. The effects of emotions on short-term power spectrum analysis of heart rate variability. Am. J. Cardiol. 76 (1995) 1089-1093
46. Mertens P.A., and Unshelm J. The effects of single and group housing on the behavior of kennelled dogs in animal shelter. Anthrozoös 9 (1996) 40-51
47. Minors S.L., and O'Grady M.R. Heart rate variability in the dog: is it too variable?. Can. J. Vet. Res. 61 (1997) 134-144
48. Mohr E., Langbein J., and Nürnberg G. Heart rate variability-a noninvasive approach to measure stress in calves and cows. Physiol. Behav. 75 (2002) 251-259
49. Normando S., Corain L., Salvadoretti M., Meers L., and Valsecchi P. Effects of an enchanced human interaction program on shelter dogs' behaviour analysed using a novel nonparametric test. Appl. Anim. Behav. Sci. 116 (2009) 211-219
50. O'Rurke R.A., Hanrath P., Henry W.N., Hugenholtz P.G., Pisa Z., Roelandt J., and Tanaka M. Report of the Joint International Society and Federation of Cardiology/World Health Organization Task Force on Recommendations for Standardization of Measurements from M-mode Echocardiograms. Circulation 69 (1984) 854A-857A
51. Palestrini C., Previde E.P., Spiezio C., and Verga M. Heart rate and behavioural responses of dogs in the Ainsworth's Strange Situation: a pilot study. Appl. Anim. Behav. Sci. 94 (2005) 75-88
52. Physick-Sheard P.W., Marlin D.J., Thornhill R., and Schroter R.C. Frequency domain analysis of heart rate variability in horses at rest and during exercise. Equine Vet. J. 32 (2000) 253-262
53. Pomfrett C.J.D., Glover D.G., Bollen B.G., and Pollard B.J. Perturbation of heart rate variability in cattle fed BSE-infected material. Vet. Rec. 154 (2004) 687-691
54. Porges S.W., Doussard-Roosevelt J.A., Portales A.L., and Greenspan S.I. Infant regulation of the vagal "Brake" predicts child behavior problems: a psychobiological model of social behavior. Dev. Psychobiol. 29 (1996) 697-712
55. Porges S.W. The polyvagal theory: phylogenetic substrates of a social nervous system. Psychoneuroendocrinology 23 (2001) 837-861
56. Rescorla R.A. Pavlovian conditioning: it's not what you think it is. Am. Psychol. 43 (1988) 151-160
57. Rietmann T.R., Stuart A.E.A., Bernasconi P., Stauffacher M., Auer J.A., and Weishaupt M.A. Assessment of mental stress in warmblood horses: heart rate variability in comparison to heart rate and selected behavioural parameters. Appl. Anim. Behav. Sci. 88 (2004) 121-136
58. Rushen J., and de Passille A.M.B. The scientific assessment of the impact of housing on animal welfare: a critical review. Can. J. Anim. Sci. 72 (1992) 712-743
59. Sahn D.J., DeMAria A., Kisslo J., and Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58 (1978) 1072-1083
60. Selye H. Diseases of adaptation and ACTH and cortisone therapy. An. R. Acad. Nac. Med. (Madr.) 67 (1950) 634-649
61. Sgoifo A., Koolhaas J.M., Musso E., and De Boer S.F. Different sympathovagal modulation of heart rate during social and nonsocial stress episodes in wild-type rats. Physiol. Behav. 67 (1999) 733-738
62. Sgoifo A., Pozzato C., Costoli T., Manghi M., Stilli D., Ferrari P.F., Ceresini G., and Musso E. Cardiac responses to intermittent social conflict in rats. Physiol. Behav. 73 (2001) 343-349
63. Siegel S. Explanatory mechanisms for placebo effects: Pavlovian conditioning. In: Guess H.A., Kleinman A., Kusek J.W., and Engel L.W. (Eds). The Science of the Placebo: Toward an Interdisciplinary Research Agenda (2002), BMJ Books, London 133-157
64. Smith R.F., and Dobson H. Hormonal interactions within the hypothalamus and pituitary with respect to stress and reproduction in sheep. Dom. Anim. Endocrinol. 23 (2002) 75-85
65. Task Force of the European Society of Cardiology, North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93 (1996) 1043-1065
66. Tiller W.A., McCraty R., and Atkinson M. Cardiac coherence: a new, noninvasive measure of autonomic nervous system order. Altern. Ther. Health Med. 2 (1996) 52-65
67. Valsecchi P., Pattacini O., Beretta V., Bertozzi J., Zannoni S., Viggiani R., and Accorsi P.A. Effects of a human social enrichment program on behaviour and welfare of sheltered dogs. J. Vet. Behav. Clin. Appl. Res. 2 (2007) 87-88
68. Van der Borg J.A.M., Netto W.J., and Planta D.J.U. Behavioural testing of dogs in animal shelters to predict problem behaviour. Appl. Anim. Behav. Sci. 32 (1991) 237-251
69. Vincent I.C., and Michell A.R. Comparison of cortisol concentrations in saliva and plasma of dogs. Res. Vet. Sci. 53 (1992) 342-345
70. Vincent I.C., and Michell A.R. Relationship between blood pressure and stress-prone temperament in dogs. Physiol. Behav. 60 (1996) 135-138
71. Visser E.K., van Reenen C.G., van der Werf J.T.N., Schilder M.B.H., Knaap J.H., Barneveld A., and Blochkuis H.J. Heart rate and heart rate variability during a novel object test and a handling test in young horses. Physiol. Behav. 76 (2002) 289-296
72. von Borell E., Langbein J., Després G., Hansen S., Leterrier C., Marchant-Forde J., Marchant-Forde R., Minero M., Mohr E., Prunier A., Valance D., and Veissier I. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals-a review. Physiol. Behav. 92 (2007) 293-316
73. Wells D.L., and Hepper P.G. The influence of environmental change on the behaviour of sheltered dogs. Appl. Anim. Behav. Sci. 68 (2000) 151-162
74. Wells D.L. A review of environmental enrichment for kenneled dogs, Canis familiaris. Appl. Anim. Behav. Sci. 85 (2004) 307-317