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Perioperative stress response in dogs undergoing elective surgery: variations in behavioural, neuroendocrine, immune and acute phase responses

Published online by Cambridge University Press:  11 January 2023

C Siracusa*
Affiliation:
Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, 3900 Delancey Street, Philadelphia, PA 19104, USA Department of Veterinary Medicine and Surgery, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
X Manteca
Affiliation:
Department of Animal Sciences and Nutrition, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
J Cerón
Affiliation:
Department of Animal Medicine and Surgery, Veterinary Faculty, University of Murcia, 30100 Murcia, Spain
S Martínez-Subiela
Affiliation:
Department of Animal Medicine and Surgery, Veterinary Faculty, University of Murcia, 30100 Murcia, Spain
R Cuenca
Affiliation:
Department of Veterinary Medicine and Surgery, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
S Lavín
Affiliation:
Department of Veterinary Medicine and Surgery, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
F Garcia
Affiliation:
Department of Veterinary Medicine and Surgery, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
J Pastor
Affiliation:
Department of Veterinary Medicine and Surgery, Veterinary Faculty, Universitat Autònoma de Barcelona, Edif V, Campus UAB, 08193 Bellaterra, Barcelona, Spain
*
* Contact for correspondence and requests for reprints: Carlo.Siracusa@uab.cat

Abstract

The aim of this trial was to describe the behavioural, neuroendocrine, immune and acute phase stress responses in dogs undergoing elective surgery in normal, clinical practice conditions. Sixteen dogs were submitted to elective orchiectomy or ovariohysterectomy using a standardised surgical protocol. Each animal was confined to the Intensive Care Unit during pre- and post-surgery and perioperative behavioural, neuroendocrine, immune and acute phase responses were studied. Behavioural categories, cortisol, prolactin, white blood cell, C-reactive protein and haptoglobin variation were evaluated. Values at different times were compared with basal values shown by the dog in its usual environment. Communicative and explorative behaviours showed high occurrence pre-surgery and were inhibited post-surgery. Decreases in post-surgery activity, interactive behaviours and changes in waking/sleeping patterns were observed. The most sensitive marker of psychological stress, cortisol, in comparison with basal values, showed a significant increase both during pre- and post-surgery confinement in the ICU cage. Prolactin values were characterised by a significant decrease early into the post-surgery period. The immune response was characterised by long-term neutrophilia and monocytosis, but by short-term lymphopaenia and eosinopaenia, limited to the early post-operative period. With regard to the acute phase response, both C-reactive protein and haptoglobin showed a long-term increase, post-surgery. Changes in behavioural, haematological and biochemical markers showed that perioperative stress represents a major challenge to dog welfare.

Type
Articles
Copyright
© 2008 Universities Federation for Animal Welfare

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References

Alleva, R, Tomasetti, M, Solenghi, MD, Stagni, F, Gamberini, F, Bassi, A, Fornasari, PM, Fanelli, G and Borghi, B 2003 Lymphocyte DNA damage precedes DNA repair or cell death after orthopaedic surgery under general anaesthesia. Mutagenesis 18: 423428CrossRefGoogle ScholarPubMed
Ambrisko, TD, Hikasa, Y and Sato, K 2005 Influence of medetomidine on stress-related neurohormonal and metabolic effects caused by butorphanol, fentanyl, and ketamine administration in dogs. The American Journal of Veterinary Research 66: 406412CrossRefGoogle ScholarPubMed
Anand, KJS, Phil, D and Hickey, PR 1992 Halothane-morphine compared with high-dose sufentanil for anaesthesia and postoperative analgesia in neonatal cardiac surgery. The New England Journal of Medicine 326: 19CrossRefGoogle ScholarPubMed
Beerda, B, Schilder, MBH, Janssen, NSCRM and Mol, JA 1996 The use of saliva cortisol and catecholamine measurements for a noninvasive assessment of stress response in dogs. Hormones and Behaviour 30: 272279CrossRefGoogle ScholarPubMed
Beerda, B, Schilder, MB, van Hooff, JARAM and de Vries, HW 1997 Manifestation of chronic and acute stress in dogs. Applied Animal Behaviour Science 52: 307319CrossRefGoogle Scholar
Beerda, B, Schilder, MB, van Hooff, JARAM, de Vries, HW and Mol, JA 1998 Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Applied Animal Behaviour Science 58: 365381CrossRefGoogle Scholar
Beerda, B, Schilder, MB, van Hooff, JARAM, de Vries, HW and Mol, JA 1999 Chronic stress in dogs subjected to social and spatial restriction I. Behavioral response. Physiology and Behavior 66: 233242CrossRefGoogle Scholar
Blackburn-Munro, G 2004 Pain-like behaviours in animals – how human are they? Trends in Pharmacological Science 25: 299305CrossRefGoogle Scholar
Blecha, F 2000 Immune system response to stress. In: Moberg, GP and Mench, JA (eds) The Biology Of Animal Stress pp 111122. CABI Publishing: Wallingford, UKGoogle Scholar
Ceròn, JJ, Eckersall, DP and Martinez-Subiela, S 2005 Acute phase proteins in dogs and cats: current knowledge and future perspectives. Veterinary Clinical Pathology 34: 8599CrossRefGoogle ScholarPubMed
Conner, JG and Eckersall, PD 1988 Acute phase response in the dog following surgical trauma. Research in Veterinary Science 45: 107110CrossRefGoogle ScholarPubMed
Coppola, CL, Grandin, T and Enns, RM 2006 Human interaction and cortisol: Can human contact reduce stress for shelter dogs? Physiology and Behavior 87: 537541CrossRefGoogle ScholarPubMed
Crowell-Davis, S and Murray, T 2006 Veterinary Psychopharmacology. Blackwell Publishing: Ames, Iowa, USAGoogle Scholar
Cuadra, G, Zurita, A, Lacerra, CMN and Molina, A 1999 Chronic stress sensitizes frontal cortex dopamine release in response to a subsequent novel stressor: reversal by naloxone. Brain Research Bulletin 48: 303308CrossRefGoogle ScholarPubMed
Dantzer, R and Mormede, P 1995 Psychoneuroimmunology of stress. In: Leonard, B and Miller, K (eds) Stress, the Immune System and Psychiatry pp 4767. John Wiley and Sons Ltd: New York, USAGoogle Scholar
Delogu, G, Moretti, S, Famularo, G, Marcellini, S, Santini, G, Antonucci, A, Marandola, M and Signore, L 2001 Mitochondrial perturbations and oxidant stress in lymphocytes from patients undergoing surgery and general anesthesia. Archives of Surgery 136: 11901196CrossRefGoogle ScholarPubMed
Desborough, JP 2000 The stress response to trauma and surgery. British Journal of Anaesthesia 85: 109117CrossRefGoogle Scholar
Devitt, CM, Cox, RE and Hailey, JJ 2005 Duration, complication, stress and pain of open ovariohysterectomy versus a simple method of laparoscopic-assisted ovariohysterectomy in dogs. Journal of Veterinary Medical Association 227: 921927CrossRefGoogle ScholarPubMed
Fox, MS, Mellor, DG, Lawoko, CRO, Hodge, H and Firth, C 1998 Changes in plasma cortisol concentrations in bitches in response to different combinations of halothane and butorphanol, with or without ovariohysterectomy. Research in Veterinary Science 65: 125133CrossRefGoogle ScholarPubMed
Giescke, K, Hamberger, B, Jamberg, PD, Klingstedt, C and Pearson, B 1988 High and low dose fentanyl anaesthesia: hormonal and metabolic response during cholecystectomy. British Journal of Anaesthesia 61: 575582CrossRefGoogle Scholar
Goodmann, PA, Klinghammer, E and Willard, J 2002 Wolf Ethogram, Ethology Series No 3. EH Hess Institute of Ethology: Battleground, USAGoogle Scholar
Griffis, CA, Compton, P and Doering, L 2006 The effect of pain on leukocyte cellular adhesion molecules. Biological Research for Nursing 7: 297312CrossRefGoogle ScholarPubMed
Hansen, BD, Hardie, EM and Carroll, GS 1997 Physiological measurements after ovariohysterectomy in dogs: what's normal? Applied Animal Behaviour Science 51: 101109CrossRefGoogle Scholar
Hardie, EM, Hansen, BD and Carrol, GS 1997 Behaviour after ovariohysterectomy in the dog: what's normal? Applied Animal Behavioural Science 51: 111128CrossRefGoogle Scholar
Hart, BL 1985 Behavioural indications for phenotiazine and benzodiazepine tranquilizers in dogs. Journal of American Veterinary Medical Association 186: 192194Google Scholar
Hetts, S, Clark Derrel, J, Calpin, JP, Arnold, CE and Mateo, JM 1992 Influence of housing conditions on beagle behaviour. Applied Animal Behavioural Science 34: 137155CrossRefGoogle Scholar
Holton, L, Reid, J, Scott, EM, Pawson, P and Nolan, A 2001 Development of a behaviour-based scale to measure acute pain in dogs. Veterinary Record 148: 525531CrossRefGoogle ScholarPubMed
Hubrecht, RC, Serpell, JA and Poole, T 1992 Correlates of pen size and housing conditions in the behaviour of kennelled dogs. Applied Animal Behavioural Science 34: 365383CrossRefGoogle Scholar
Kobelt, AJ, Hemsworth, PH, Barnett, JL and Butler, KL 2003 Sources of sampling variation in saliva cortisol in dogs. Research in Veterinary Science 75: 157161CrossRefGoogle ScholarPubMed
Mandel, I 1990 The diagnostic use of saliva. Journal of Oral Phatology Medicine 19: 119125CrossRefGoogle ScholarPubMed
Marrocco-Trischitta, MM, Tiezzi, A, Svampa, MG, Bandiera, G, Camilli, S, Stillo, F, Petasecca, P, Sampogna, F, Abeni, D and Gurrini, P 2004 Perioperative stress response to carotid endarterectomy: the impact of anaesthetic modality. Journal of Vascular Surgery 39: 12951304CrossRefGoogle Scholar
Martin, P and Bateson, P 1993 Measuring Behaviour: An Introductory Guide, Second Edition. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Mason, WA 2000 Early developmental influences of experience on behavior, temperament and stress. In: Moberg, GP and Mench, JA (eds) The Biology Of Animal Stress pp 269290. CABI Publishing: Wallingford, UKGoogle Scholar
Mathews, KA 2000 Pain assessment and general approach to management. Veterinary Clinics of North America: Small Animal Practice 30: 729755CrossRefGoogle ScholarPubMed
Matteri, RL, Carroll, JA and Dyer, CJ 2000 Neuroendocrine response to stress. In: Moberg, GP and Mench, JA (eds) The Biology Of Animal Stress pp 4376. CABI Publishing: Wallingford, UKGoogle Scholar
Mellor, DJ, Cook, CJ and Stafford, KJ 2000 Quantifying some responses to pain as a stressor. In: Moberg, GP and Mench, JA (eds) The Biology Of Animal Stress pp 171198. CABI Publishing: Wallingford, UKGoogle Scholar
Moberg, GP 2000 Biological response to stress: implications for animal welfare.In: Moberg GP and Mench JA (eds) The Biology Of Animal Stress pp 122. CABI Publishing: Wallingford, UKGoogle Scholar
Morton, DB and Griffiths, PHM 1985 Guidelines on the recognition of pain, distress and discomfort in experimental animals and a hypothesis for assessment. Veterinary Record 20: 431436CrossRefGoogle Scholar
Morton, CM, Reid, J, Scott, EM, Holton, LL and Nolan, AM 2005 Application of a scaling model to establish and validate an interval level pain scale for assessment of acute pain in dogs. American Journal of Veterinary Research 66: 21542166CrossRefGoogle ScholarPubMed
Murata H, Shimada H and Yoshioka 2004 Current research on acute phase proteins in veterinary diagnosis: an overview. The Veterinary Journal 168: 2840CrossRefGoogle Scholar
Odendaal, JS and Meintjes, RA 2003 Neurophysiological correlates of affiliative behaviour between humans and dogs. The Veterinary Journal 165: 296301CrossRefGoogle ScholarPubMed
Pageat, P 1998 Pathologie Du Comportement Du Chien, Second Edition. Le Point Vétérinaire: Maisons-Alfort, France. [Title translation: Behavioural Pathology in the Dog]Google Scholar
Pageat P and Gaultier 2003 Using prolactin blood level in the diagnosis of anxiety related disorders in dogs. In: Heath, S and DeKeuster, T (eds) Therapeutic Approaches in Veterinary Behavioural Medicine. Proceedings of the Ninth ESVCE Congress pp 3536. 19 September 2003, Salzburg, Austria. ESVCE: Lovendegem, BelgiumGoogle Scholar
Pageat, P 2005 Assessing prolactinemia in anxious dogs (Canis familiaris): interest in diagnostic value and use in the selection of the most appropriate psychotropic drug. In: Mills D, Levine E, Landsberg G, Horwitz D, Duxbury M, Mertens P, Meyer X, Huntley LR, Reich M and Willard J (eds) Current Issues and Research in Veterinary Behavioural Medicine. Papers presented at the Fifth International Behaviour Meeting. 14-16 July 2005, West Lafayette, Indiana, USA: Purdue University Press, USAGoogle Scholar
Pageat, P, Lafont, C, Falewée, C, Bonnafous, L, Gaultier, E and Sillart, B 2007 An evaluation of serum prolactin in anxious dogs and response to treatment with selegiline or fluoxetine. Applied Animal Behaviour Science 105: 342350CrossRefGoogle Scholar
Roughan, JV and Flecknell, PA 2002 Buprenorphine: a reappraisal of its antinociceptive effects and therapeuric use in alleviating post-operative pain in animals. Laboratory Animals 36: 322343CrossRefGoogle Scholar
Roughan, JV and Flecknell, PA 2003 Evaluation of a short duration behaviour-based post-operative pain scoring system in rats. European Journal of Pain 7: 397406CrossRefGoogle Scholar
Rushen, J 2000 Some issues in the interpretation of behavioural response to stress. In: Moberg, GP and Mench, JA (eds) The Biology Of Animal Stress pp 2341. CABI Publishing: Wallingford, UKGoogle Scholar
Sanford, J, Ewbank, R, Molony, V, Tavernor, WD and Uvarov, O 1986 Guidelines for the recognition and assessment of pain in animals. Veterinary Record 118: 334338Google Scholar
Schultze, AE 2000 Interpretation of canine leukocyte responses. In: Feldman, BJ, Zinkl, JG and Jain, NC (eds) Shalm's Veterinary Ematology pp 366381. Lippincott Williams and Wilkins: Baltimora, USAGoogle Scholar
Sibanda, S, Hughes, JM, Pawson, PE, Kelly, G and Bellenger, CR 2006 The effects of preoperative extradural bupivocaine and morphine on the stress response in dogs undergoing femoro-tibial joint surgery. Veterinary Anaesthesia and Analgesia 33: 246257CrossRefGoogle Scholar
Stockham, SL, Keeton, KS and Szlatovits, B 2003 Clinical assessment of leukocytosis: distinguishing leukocytoses caused by inflammatory, glucocorticoid, physiologic and leukemic disorders or conditions. Veterinary Clinics of North America: Small Animal Practice 33: 13351357CrossRefGoogle ScholarPubMed
Stover, SM, Steffey, EP, Dybdal, NO and Franti, CE 1998 Hematologic and serum biochemical alterations associated with multiple halothane anesthesia exposures and minor surgical trauma in horses. American Journal of Veterinary Research 49: 236241Google Scholar
Tayama, E, Hayashida, N, Oda, T, Tomoeda, H, Akasu, K, Kosuga, T, Fukunaga, S, Akashi, H, Kawara, T and Aoyagi, S 1999 Recovery from lymphocytopenia following extracorporeal circulation: simple indicator to assess surgical stress. Artificial Organs 23: 736740CrossRefGoogle ScholarPubMed
Taylor, PM 1998 Effects of surgery on endocrine and metabolic responses to anaesthesia in horses and ponies. Research in Veterinary Science 64: 133140CrossRefGoogle Scholar
Thompson, SB 1998 Pharmacological treatment of phobias. In: Dodman, NH and Shuster, L (eds) Psychopharmacology of Animal Behaviour Disorders pp 141184. Blackwell Science Inc: Malden, USAGoogle Scholar
Väisänen, MN, Raekallio, M, Kuusela, E, Huttumen, P, Leppäluoto, J, Kirves, P and Vainio, O 2002 Evaluation of the perioperative stress response in dogs administered medetomidine or acepromazine as part of the preanesthetic medication. American Journal of Veterinary Research 63: 969975CrossRefGoogle ScholarPubMed
Väisänen, MA, Valros, AE, Hakaoja, E, Raekallio, MR and Vainio, OM 2005 Pre-operative stress in dogs: a preliminary investigation of behaviour and heart rate variability in healthy hospitalized dogs. Veterinary Anaesthesia and Analgesia 32: 158167CrossRefGoogle ScholarPubMed
Vetter, TR and Heiner, EJ 1996 Discordance between patient self reported visual analogue scale pain scores and observed pain-related behavior in older children after surgery. Journal of Clinical Anesthesia 8: 371375CrossRefGoogle ScholarPubMed
Wells, DL 2004 A review of environmental enrichment for kennel dogs, Canis familiaris. Applied Animal Behaviour Science 85: 307317CrossRefGoogle Scholar
Yamamoto, S, Shida, T, Miyaji, S, Santsuka, H, Fuise, H, Mukawa, K, Furukawa, E, Nagae, T and Naiki, M 1993 Changes in serum C-reactive protein levels in dogs with various disorders and surgical traumas. Veterinary Research Communications 17: 8593CrossRefGoogle ScholarPubMed
Zahorec, R 2001 Ratio of neutrophil to lymphocyte counts: rapid and simple parameter of systemic inflammation and stress in critically ill. Bratislava Medical Journal 102: 514Google ScholarPubMed
Zakowsi, SG, McAllister, CG, Deal, M and Baum, A 1992 Stress, reactivity, and immune function in healthy men. Health Psychology 11: 223232CrossRefGoogle Scholar