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A multiparametric approach to discriminate the impacts of different degrees of invasiveness of surgical procedures in sheep

  • M. Faure (a1) (a2), V. Paulmier (a1), A. Boissy (a1) (a2), A. de La Foye (a1) (a2), A. de Boyer Des Roches (a1) (a2) and D. Durand (a1) (a2)...


Traumatic situations in animals induce responses including pain, expressed through behavioural and physiological pathways such as inflammation, oxidative stress, hypothalamic–pituitary–adrenal (HPA) axis and autonomic nervous system. As some of these systems can also be activated during excitement and situations with a positive valence, their use as a means to assess pain response is difficult. We explored (i) how these five aforementioned pathways change in sheep exposed to various degrees of invasiveness of surgical procedures despite a therapeutic regimen and (ii) whether a multiparametric analysis that combines information from these five pathways enhances the discrimination between these situations, and estimates the relative importance of these pathways in the response. We used 24 adult sheep split into four treatments: Control (C; no fasting, no anaesthesia, no surgery), Sham (S; fasting, anaesthesia, no surgery), Rumen Canulation (R; fasting, anaesthesia, rumen cannulation) and Rumen–Duodenal–Ileum cannulation (RDI; fasting, anaesthesia, cannulation of the rumen, duodenum and ileum). Sheep’ responses were measured for 5 days after surgery. When considering each behavioural or physiological pathway independently, discrimination between treatments was acceptable, its sensitivity (Se) ranging from 0% to 100%, and its specificity (Sp) ranging from 62% to 100%. The multiparametric analysis gathering information from the five pathways enhanced the effectiveness of discrimination between treatments (Se, 50% to 100%; Sp, 82% to 100%), and gave additional information on the relative contribution of each pathway to the global sheep response. Sheep global response was higher when exposed to a surgery, and increased with the surgery invasiveness. This response relied mostly on inflammation (absolute correlation for haptoglobin, 0.89), HPA (cortisol, 0.85) and behaviour (antalgic postures, 0.85). The multiparametric approach seems to be a promising tool to discriminate between different degrees of invasiveness of surgical procedures.


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Arlot, S and Celisse, A 2010. A survey of cross-validation procedures for model selection. Statistics Surveys 4, 40-79.
Auboiron, S, Sparrow, DA, Beaubatie, L, Bauchart, D, Sparrow, JT, Laplaud, PM and Chapman, MJ 1990. Characterization and amino-terminal sequence of apolipoprotein AI from plasma high density lipoproteins in the preruminant calf, Bos spp. Biochemical and Biophysical Research Communication 166, 833839.
Boissy, A and Bouissou, MF 1994. Effects of androgen treatment on behavioral and physiological responses of heifers to fear-eliciting situations. Hormones and Behavior 28, 6683.
Bussières, G, Jacques, C, Lainay, O, Beauchamp, G, Leblond, A, Cadoré, JL, Desmaizières, LM, Cuvelliez, SG and Troncy, E 2008. Development of a composite orthopaedic pain scale in horses. Research in Veterinary Science 85, 294306.
de Oliveira, FA, Luna, SPL, do Amaral, JB, Rodrigues, KA, Sant’Anna, AC, Daolio, M and Brondani, JT 2014. Validation of the UNESP-Botucatu unidimensional composite pain scale for assessing postoperative pain in cattle. BMC Veterinary Research 10, 114.
Earley, B and Crowe, MA 2002. Effects of ketoprofen alone or in combination with local anesthesia during the castration of bull calves on plasma cortisol, immunological, and inflammatory responses. Journal of Animal Science 80, 10441052.
Fisher, AD, Verkerk, GA, Morrow, CJ and Matthews, LR 2002. The effects of feed restriction and lying deprivation on pituitary–adrenal axis regulation in lactating cows. Livestock Production Science 73, 255263.
Gadek-Michalska, A, Spyrka, J and Bugajski, J 2005. Psychosocial stress affects the involvement of prostaglandins and nitric oxide in the lipopolysaccharide-induced hypothalamic-pituitary-adrenal response. Journal of Physiology and Pharmacology 56, 287298.
Gobert, M, Martin, B, Ferlay, A, Chilliard, Y, Graulet, B, Pradel, P, Bauchart, D and Durand, D 2009. Plant polyphenols associated with vitamin E can reduce plasma lipoperoxidation in dairy cows given n-3 polyunsaturated fatty acids. Journal of Dairy Science 92, 60956104.
Graubner, C, Gerber, V, Doherr, M and Spadavecchia, C 2011. Clinical application and reliability of a post abdominal surgery pain assessment scale (PASPAS) in horses. The Veterinary Journal 188, 178183.
GrØndahl-Nielsen, C, Simonsen, HB, Damkjer Lund, J and Hesselholt, M 1999. Behavioural, endocrine and cardiac responses in young calves undergoing dehorning without and with use of sedation and analgesia. The Veterinary Journal 158, 1420.
Guesgen, MJ, Beausoleil, NJ, Minot, EO, Stewart, M, Stafford, KJ and Morel, PCH 2016. Lambs show changes in ear posture when experiencing pain. Animal Welfare 25, 171177.
Güllner, H-G 1983. Prostaglandin actions on the adrenergic nervous system. Klinische Wochenschrift 61, 533540.
Kanehisa, M 1988. A multivariate analysis method for discriminating protein secondary structural segments. Protein Engineering 2, 8792.
Kent, JE, Molony, V and Robertson, IS 1993. Changes in plasma cortisol concentration in lambs of three ages after three methods of castration and tail docking. Research in Veterinary Science 55, 246251.
Lebart, L, Piron, M and Morineau, A 1995. Statistique exploratoire multidimensionnelle. Dunod, 456 p.
Lonardi, C, Scollo, A, Normando, S, Brscic, M and Gottardo, F 2015. Can novel methods be useful for pain assessment of castrated piglets? Animal 9, 871877.
Lykkesfeldt, J and Svendsen, O 2007. Oxidants and antioxidants in disease: oxidative stress in farm animals. The Veterinary Journal 173, 502511.
Martin, P and Bateson, P 2013. Measuring behaviour: an introductory guide. Cambridge University Press, 186 p.
Martin, J and White, H 1991. Fluorimetric determination of oxidized and reduced glutathione in cells and tissues by high performance liquid chromatography following derivatization with dansyl chloride. Journal of Chromatography 568, 219225.
McLennan, KM, Rebelo, CJB, Corke, MJ, Holmes, MA, Leach, MC and Constantino-Casas, F 2016. Development of a facial expression scale using footrot and mastitis as models of pain in sheep. Applied Animal Behaviour Science 176, 1926.
Melches, S, Mellema, SC, Doherr, MG, Wechsler, B and Steiner, A 2007. Castration of lambs: A welfare comparison of different castration techniques in lambs over 10 weeks of age. The Veterinary Journal 173, 554563.
Molony, V and Kent, JE 1997. Assessment of acute pain in farm animals using behavioral and physiological measurements. Journal of Animal Science 75, 266272.
Molony, V, Kent, JE and McKendrick, IJ 2002. Validation of a method for assessment of an acute pain in lambs. Applied Animal Behaviour Science 76, 215238.
Payne, WW and Poulton, EP 1923. Visceral pain in the upper alimentary tract. Quarterly Journal of Medicine 65, 5380.
Perrière, G and Thioulouse, J 2003. Use of correspondence discriminant analysis to predict the subcellular location of bacterial proteins. Computer Methods and Programs in Biomedicine 70, 99105.
Prunier, A, Mounier, L, Le Neindre, P, Leterrier, C, Mormede, P, Paulmier, V, Prunet, P, Terlouw, C and Guatteo, R 2013. Identifying and monitoring pain in farm animals: a review. Animal 7, 9981010.
Rialland, P, Otis, C, de Courval, ML, Mulon, PY, Harvey, D, Bichot, S, Gauvin, D, Livingston, A, Beaudry, F, Hélie, P, Frank, D, del Castillo, JRE and Troncy, E 2014. Assessing experimental visceral pain in dairy cattle: a pilot, prospective, blinded, randomized, and controlled study focusing on spinal pain proteomics. Journal of Dairy Science 97, 21182134.
Röhrig, B, du Prel, J-B, Wachtlin, D, Kwiecien, R and Blettner, M 2010. Sample size calculation in clinical trials. Deutsches Arzteblatt 107, 552556.
Ruzic, B, Tomaskovic, I, Trnski, D, Kraus, O, Bekavac-Beslin, M and Vrkic, N 2005. Systemic stress responses in patients undergoing surgery for benign prostatic hyperplasia. BJU International 95, 7780.
Salvemini, D, Little, JW, Doyle, T and Neumann, WL 2011. Roles of reactive oxygen and nitrogen species in pain. Free Radical Biology & Medicine 51, 951966.
Stafford, KJ and Mellor, DJ 2005. Dehorning and disbudding distress and its alleviation in calves. The Veterinary Journal 169, 337349.
Valverde, A and Gunkel, CI 2005. Pain management in horses and farm animals. Journal of Veterinary Emergency and Critical Care 15, 295307.
Veissier, I and Boissy, A 2007. Stress and welfare: two complementary concepts that are intrinsically related to the animal’s point of view. Physiology & Behavior 92, 429433.
Vinuela-Fernandez, I, Jones, E, Welsh, EM and Fleetwood-Walker, SM 2007. Pain mechanisms and their implication for the management of pain in farm and companion animals. Veterinary Journal 174, 227239.


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A multiparametric approach to discriminate the impacts of different degrees of invasiveness of surgical procedures in sheep

  • M. Faure (a1) (a2), V. Paulmier (a1), A. Boissy (a1) (a2), A. de La Foye (a1) (a2), A. de Boyer Des Roches (a1) (a2) and D. Durand (a1) (a2)...


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