Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T20:18:26.722Z Has data issue: false hasContentIssue false

Hair cortisol concentrations in New Zealand white rabbits subjected to surgery

Published online by Cambridge University Press:  03 January 2023

T Peric*
Affiliation:
Department of Agri-Food, Animal and Environmental Sciences, University of Udine, Via delle Scienze 206, 33100 Udine, Italy
A Comin
Affiliation:
Department of Agri-Food, Animal and Environmental Sciences, University of Udine, Via delle Scienze 206, 33100 Udine, Italy
M Corazzin
Affiliation:
Department of Agri-Food, Animal and Environmental Sciences, University of Udine, Via delle Scienze 206, 33100 Udine, Italy
M Montillo
Affiliation:
Department of Agri-Food, Animal and Environmental Sciences, University of Udine, Via delle Scienze 206, 33100 Udine, Italy
F Canavese
Affiliation:
Hôpital Estaing, CHU of Clermont Ferrand, Place Lucie et Raymond Aubrac, 63100 Clermont-Ferrand, France
M Stebel
Affiliation:
Department of Life Sciences, University of Trieste, Via Giorgieri 1, 34127 Trieste, Italy
A Prandi
Affiliation:
Department of Agri-Food, Animal and Environmental Sciences, University of Udine, Via delle Scienze 206, 33100 Udine, Italy
*
* Contact for correspondence and requests for reprints: [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.

The aim of this study was to assess hair cortisol concentrations in New Zealand white rabbits (Oryctolagus cuniculus) that were subjected to relocation and surgery to evaluate HPA-axis activity; in addition, we used this marker of cortisol secretion to evaluate the allostatic load of animals undergoing surgery. After a period of acclimatisation, which lasted 40 days from their arrival at the enclosure, 19 rabbits were subjected to T1-T12 dorsal arthrodesis (RS), 19 were sham-operated (SS), and 19 were non-operated (CON). Hair samples were collected at the time of arrival (ST1) at the animal facility, and seven other sets of hair samples were collected at 40-day intervals from the same area of skin for a period of 240 days as re-shaved hair (anagen phase): immediately before surgery (ST2) and after the surgery (ST3, ST4, ST5, ST6, ST7, and ST8). The transition from the rabbitry to the animal breeding facility led to a significant increase in cortisol concentration (ST2) in all of the groups. At ST3, the RS group presented higher cortisol concentrations than those of the SS group and the CON group. At ST4, the experimental groups showed similar values that remained constant until ST8. The results show that the management of rabbits undergoing surgery should be evaluated very carefully, and hair cortisol concentrations may provide a means of avoiding the dangerous cumulative effects of additional stressors close to surgery.

Type
Research Article
Copyright
© 2018 Universities Federation for Animal Welfare

References

Accorsi, PA, Carloni, E, Valsecchi, P, Viggiani, R, Gamberoni, M, Tamanini, C and Seren, E 2008 Cortisol determination in hair and faeces from domestic cats and dogs. General and Comparative Endocrinology 155(2): 398402. https://doi.org/10.1016/j.ygcen.2007.07.002CrossRefGoogle ScholarPubMed
Balikova, M 2005 Hair analysis for drugs of abuse. Plausibility of interpretation. Biomedical Papers of the Medical Faculty of the University Palacký, Olomouc, Czechoslovakia 149: 199207. https://doi.org/10.5507/bp.2005.026CrossRefGoogle ScholarPubMed
Barone, R 1996-2004 Anatomie Comparée des Mammifères Domestiques. Tome 1-6. Vigot Frères Editeurs: Paris, FranceGoogle Scholar
Batchelor, GR 1999 The laboratory rabbit. In: Poole, T (ed) The UFAW Handbook on the Care and Management of Laboratory Animals, Seventh Edition pp 395408. Blackwell Science: Oxford, UKGoogle Scholar
Baumans, V 2004 The welfare of laboratory mice. In: Kaliste, E (ed) The Welfare of Laboratory Animals pp 119152. Kluwer Academic Publishers: Dordrecht: The Netherlands. https://doi.org/10.1007/978-1-4020-2271-5_7CrossRefGoogle Scholar
Bennett, A and Hayssen, V 2010 Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domestic Animal Endocrinology 39(3): 171180. https://doi.org/10.1016/j.domaniend.2010.04.003CrossRefGoogle ScholarPubMed
Bévalot, F, Gaillard, Y, Lhermitte, MA and Pépin, G 2000 Analysis of corticosteroids in hair by liquid chromatography-elec-trospray ionization mass spectrometry. Journal of Chromatography. B, Biomedical Sciences and Applications 740(2): 227236. https://doi.org/10.1016/S0378-4347(00)00085-2CrossRefGoogle Scholar
Canavese, F, Dimeglio, A, Barbetta, D, Pereira, B, Fabbro, S, Bassini, F and Canavese, B 2014 Effect of thoracic arthrode-sis in prepubertal New Zealand white rabbits on cardio-pul-monary function. Indian Journal of Orthopaedics 48: 184192. https://doi.org/10.4103/0019-5413.128763CrossRefGoogle ScholarPubMed
Canavese, F, Dimeglio, A, D’Amato, C, Volpatti, D, Granier, M, Stebel, M, Cavalli, F and Canavese, B 2010 Dorsal arthrodesis in prepubertal New Zealand White rabbits followed to skeletal maturity: effect on thoracic dimensions, spine growth and neural elements. Indian Journal of Orthopaedics 44: 1422. https://doi.org/10.4103/0019-5413.57280CrossRefGoogle ScholarPubMed
Canavese, F, Dimeglio, A, Granier, M, Beraldo, P, Bonnel, F, Stebel, M, Daures, JP, Canavese, B and Cavalli, F 2008 Influence de l'arthrodèse vertébrale sélective T1- T6 sur la crois-sance thoracique: étude expérimentale chez des lapins New Zealand white prépubertaires. Revue de Chirurgie Orthopédique et Réparatrice de L'appareil Moteur 94: 490497. [Title translation: Selective dorsal T1-T6 fusion of the thoracic spine and effects on thorax growth: experimental study in pre-pubertal New Zealand white rabbits]. https://doi.org/10.1016/j.rco.2008.04.002CrossRefGoogle Scholar
Canavese, F, Dimeglio, A, Stebel, M, Galeotti, M, Canavese, B and Cavalli, F 2013 Thoracic cage plasticity in prepubertal New Zealand white rabbits submitted to T1-T12 dorsal arthrode-sis: Computed tomography evaluation, echocardiographic assess-ment and cardio-pulmonary measurements. European Spine Journal: Official Publication of the European Spine Society, the European Spinal Deformity Society, and the European Section of the Cervical Spine Research Society 22: 11011112CrossRefGoogle Scholar
Canavese, F, Dimeglio, A, Volpatti, D, Stebel, M, Daures, JP, Canavese, B and Cavalli, F 2007 Dorsal arthrodesis of thoracic spine and effects on thorax growth in prepubertal New Zealand white rabbits. Spine 32: E443E450. https://doi.org/10.1097/BRS.0b013e3180bc2340CrossRefGoogle ScholarPubMed
Castaneda, S, Largo, R, Calvo, E, Rodríguez-Salvanés, F, Marcos, ME, Díaz-Curiel, M and Herrero-Beaumont, G 2006 Bone mineral measurements of subchondral and trabecular bone in healthy and osteoporotic rabbits. Skeletal Radiology 35: 3441. https://doi.org/10.1007/s00256-005-0022-zCrossRefGoogle ScholarPubMed
Cattet, M, Macbeth, BJ, Janz, DM, Zedrosser, A, Swenson, JE, Dumond, M and Stenhouse, GB 2014 Quantifying long-term stress in brown bears with the hair cortisol concentration: a bio-marker that may be confounded by rapid changes in response to capture and handling. Conservation Physiology 2: cou026CrossRefGoogle Scholar
Chen, Y and Lyga, J 2014 Brain-skin connection: stress, inflam-mation and skin aging. Inflammation & Allergy Drug Targets 13(3): 177190. https://doi.org/10.2174/1871528113666140522104422CrossRefGoogle Scholar
Cirimele, V, Kintz, P, Dumestre, V, Goullé, JP and Ludes, B 2000 Identification of ten corticosteroids in human hair by liquid chromatography-ionspray mass spectrometry. Forensic Science International 107(1-3): 381388. https://doi.org/10.1016/S0379-0738(99)00180-2CrossRefGoogle Scholar
Comin, A, Peric, T, Montillo, M, Faustini, M, Zufferli, V, Cappa, A, Cornacchia, G and Prandi, A 2012a Hair cortisol levels to monitor hypothalamic-pituitary-adrenal axis activity in healthy dairy cows. Journal of Animal and Veterinary Advances 11:36233626. https://doi.org/10.3923/javaa.2012.3623.3626Google Scholar
Comin, A, Zufferli, V, Peric, T, Canavese, F, Barbetta, D and Prandi, A 2012b Hair cortisol levels determined at different body sites in the New Zealand white rabbit. World Rabbit Science 20:149154. https://doi.org/10.4995/wrs.2012.1106CrossRefGoogle Scholar
D’Anna-Hernandez, KL, Ross, RG, Natvig, CL and Laudenslager, ML 2011 Hair cortisol levels as a retrospective marker of hypothalamic-pituitary axis activity throughout preg-nancy: comparison to salivary cortisol. Physiology & Behavior 104:348353. https://doi.org/10.1016/j.physbeh.2011.02.041CrossRefGoogle Scholar
Davenport, MD, Lutz, CK, Tiefenbacher, S, Novak, MA and Meyer, JS 2008 A rhesus monkey model of self-injury: effects of relocation stress on behavior and neuroendocrine function. Biological Psychiatry 63: 990996. https://doi.org/10.1016/j.biopsy-ch.2007.10.025CrossRefGoogle ScholarPubMed
Davenport, MD, Tiefenbacher, S, Lutz, CK, Novak, MA and Meyer, JS 2006 Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. General and Comparative Endocrinology 147: 255261. https://doi.org/10.1016/j.ygcen.2006.01.005CrossRefGoogle ScholarPubMed
Dettmer, AM, Novak, MA, Suomi, SJ and Meyer, JS 2012 Physiological and behavioral adaptation to relocation stress in dif-ferentially reared rhesus monkeys: hair cortisol as a biomarker for anxiety-related responses. Psychoneuroendocrinology 37: 191199. https://doi.org/10.1016/j.psyneuen.2011.06.003CrossRefGoogle ScholarPubMed
Deuss, U, Dietrich, J, Kaulen, D, Frey, K, Spangenberger, W, Allolio, B, Matuszczak, M, Troidl, H and Winkelmann, W 1994 The stress response to laparoscopic cholecystectomy: investigation of endocrine parameters. Endoscopy 26: 235238. https://doi.org/10.1055/s-2007-1008950CrossRefGoogle ScholarPubMed
Drummond, DS 1988 Harrington instrumentation with spinous process wiring for idiopathic scoliosis. The Orthopedic Clinics of North America 19: 281CrossRefGoogle ScholarPubMed
Dubois, M, Pickar, D, Cohen, MR, Roth, YF, Macnamara, T and Bunney, WE Jr 1981 Surgical stress in humans is accompa-nied by an increase in plasma beta-endorphin immunoreactivity. Life Sciences 29: 12491254. https://doi.org/10.1016/0024-3205(81)90230-7CrossRefGoogle Scholar
Fairbanks, LA, Jorgensen, MJ, Bailey, JN, Breidenthal, SE, Grzywa, R and Laudenslager, ML 2011 Heritability and genet-ic correlation of hair cortisol in vervet monkeys in low and high-er stress environments. Psychoneuroendocrinology 36: 12011208. https://doi.org/10.1016/j.psyneuen.2011.02.013CrossRefGoogle Scholar
Gaillard, Y, Vayssette, F and Pépin, G 2000 Compared inter-est between hair analysis and urinalysis in doping controls. Results for amphetamines, corticosteroids and anabolic steroids in racing cyclists. Forensic Science International 107(1-3): 361379. https://doi.org/10.1016/S0379-0738(99)00179-6CrossRefGoogle Scholar
Gibbison, B, Angelini, GD and Lightman, SL 2013 Dynamic output and control of the hypothalamic-pituitary-adrenal axis in critical illness and major surgery. British Journal of Anaesthesia 111:347360. https://doi.org/10.1093/bja/aet077CrossRefGoogle ScholarPubMed
Grass, J, Kirschbaum, C, Miller, R, Gao, W, Steudte-Schmiedgen, S and Stalder, T 2015 Sweat-inducing physiolog-ical challenges do not result in acute changes in hair cortisol con-centrations. Psychoneuroendocrinology 53: 108116. https://doi.org/10.1016/j.psyneuen.2014.12.023CrossRefGoogle ScholarPubMed
Gygax L, Neuffer I, Kaufmann C, Hauser R and Wechsler 2006 Milk cortisol concentration in automatic milking systems compared with auto-tandem milking parlors. Journal of Dairy Science 89: 34473454CrossRefGoogle Scholar
Haxholdt, OST, Kehlet, H and Dyrberg, V 1981 Effect of fentanyl on the cortisol and hyperglycemic response to abdominal surgery. Acta Anaesthesiologica Scandinavica 25: 434436. https://doi.org/10.1111/j.1399-6576.1981.tb01681.xCrossRefGoogle ScholarPubMed
Ilçöl, YO, Ozyurt, G, Kilicturgay, S, Uncu, G and Ulus, IH 2002 The decline in serum choline concentration in humans during and after surgery is associated with the elevation of cortisol, adrenocorticotropic hormone, prolactin and beta-endorphin con-centrations. Neuroscience Letters 324: 4144. https://doi.org/10.1016/S0304-3940(02)00171-4CrossRefGoogle Scholar
Ilçöl, YO, Yilmaz, Z and Ulus, IH 2003 Serum free and phos-pholipid-bound choline decrease after surgery and methylpred-nisolone administration in dogs. Neuroscience Letters 339: 195198. https://doi.org/10.1016/S0304-3940(03)00035-1CrossRefGoogle Scholar
Ito, N, Ito, T, Kromminga, A, Bettermann, A, Takigawa, M, Kees, F, Straub, RH and Paus, R 2005 Human hair follicles display a functional equivalent of the hypothalamic–pituitary–adrenal axis and synthesize cortisol. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 19: 13321334. https://doi.org/10.1096/fj.04-1968fjeCrossRefGoogle ScholarPubMed
Kehlet, H 1999 Surgical stress response: does endoscopic sur-gery confer an advantage? World Journal of Surgery 23: 801807. https://doi.org/10.1007/s002689900583CrossRefGoogle Scholar
Kilkenny, C, Browne, WJ, Curthill, IC, Emerson, M and Altman, DG 2010 Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biology 8: e1000412. https://doi.org/10.1371/journal.pbio.1000412CrossRefGoogle ScholarPubMed
Kirschbaum, C, Tietze, A, Skoluda, N and Dettenborn, L 2009 Hair as a retrospective calendar of cortisol production-Increased cortisol incorporation into hair in the third trimester of pregnancy. Psychoneuroendocrinology 34(1): 3237. https://doi.org/10.1016/j.psyneuen.2008.08.024CrossRefGoogle ScholarPubMed
Manenschijn, L, Koper, JW, Lamberts, SWJ and van Rossum, EFC 2011 Evaluation of a method to measure long term cortisol levels. Steroids 76: 10321036. https://doi.org/10.1016/j.steroids.2011.04.005CrossRefGoogle ScholarPubMed
McEwen, BS 1998 Stress, adaptation, and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences 840: 3344. https://doi.org/10.1111/j.1749-6632.1998.tb09546.xCrossRefGoogle ScholarPubMed
McEwen, BS and Wingfield, JC 2003 The concept of allostasis in biology and biomedicine. Hormones and Behavior 43: 215. https://doi.org/10.1016/S0018-506X(02)00024-7CrossRefGoogle ScholarPubMed
McEwen, BS and Wingfield, JC 2010 What is in a name? Integrating homeostasis, allostasis and stress. Hormones and Behavior 57: 105111. https://doi.org/10.1016/j.yhbeh.2009.09.011CrossRefGoogle Scholar
Meyer, JS and Novak, MA 2012 Mini-review: Hair cortisol. A novel biomarker of hypothalamic-pituitary-adrenocortical activity. Endocrinology 153: 41204127. https://doi.org/10.1210/en.2012-1226CrossRefGoogle Scholar
Minton, JE 1994 Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. Journal of Animal Science 72: 18911898. https://doi.org/10.2527/1994.7271891xCrossRefGoogle ScholarPubMed
Montagna, W and Ellis, RA 1958 The Biology of Hair Growth. Academic Press Inc: New York, USAGoogle Scholar
Negrao, JA, Porcionato, MA, de Passillé, AM and Rushen, J 2004 Cortisol in saliva and plasma of cattle after ACTH adminis-tration and milking. Journal of Dairy Science 87: 17131718. https://doi.org/10.3168/jds.S0022-0302(04)73324-XCrossRefGoogle Scholar
Noppe, G, van Rossum, EF, Vliegenthart, J, Koper, JW and van den Akker, EL 2014 Elevated hair cortisol concentrations in children with adrenal insufficiency on hydrocortisone replace-ment therapy. Clinical Endocrinology 81(6): 820825. https://doi.org/10.1111/cen.12551CrossRefGoogle Scholar
Park, E, Cho, M and Ki, CS 2009 Correct use of repeated-meas-ures analysis of variance. The Korean Journal of Laboratory Medicine 29: 19. https://doi.org/10.3343/kjlm.2009.29.1.1Google ScholarPubMed
Paus, R and Foitzik, K 2004 In search of the ‘hair cycle clock’: a guided tour. Differentiation; Research in Biological Diversity 72: 489511CrossRefGoogle Scholar
Pereg, D, Gow, R, Mosseri, M, Lishner, M, Rieder, M, Van Uum, S and Koren, G 2011 Hair cortisol and the risk for acute myocardial infarction in adult men. Stress 14: 7381. https://doi.org/10.3109/10253890.2010.511352CrossRefGoogle ScholarPubMed
Peric, T, Comin, A, Corazzin, M, Montillo, M, Canavese, F, Stebel, M and Prandi, A 2017 Relocation and hair cortisol con-centrations in New Zealand white rabbits. Journal of Applied Animal Welfare Science 20(1): 18. https://doi.org/10.1080/10888705.2016.1183489CrossRefGoogle Scholar
Popescu, C and Höcker, H 2007 Hair-the most sophisticated biological composite material. Chemical Society Reviews 36(8): 12821291. https://doi.org/10.1039/b604537pCrossRefGoogle ScholarPubMed
Rees, M, Bowen, JC, Payne, JG and MacPhee, AA 1983 Plasma beta-endorphin immunoreactivity in dogs during anes-thesia, surgery, Escherichia coli sepsis, and naloxone therapy. Surgery 93: 386390Google Scholar
Resina, J and Ferriera-Alves, A 1977 A technique of correction and internal fixation for scoliosis. The Journal of bone and joint sur-gery. British Volume 59: 159164CrossRefGoogle ScholarPubMed
Rony, HR, Cohen, DM and Schaffner, I 1953 Patterns of hair growth cycles in the colored rabbit and their modification by experimental means. The Journal of Investigative Dermatology 21:313330. https://doi.org/10.1038/jid.1953.109CrossRefGoogle ScholarPubMed
Russell, E, Koren, G, Rieder, M and Van Uum, S 2012 Hair cortisol as a biological marker of chronic stress: current status, future directions and unanswered questions. Psychoneuroendocrinology 37: 589601. https://doi.org/10.1016/j.psyneuen.2011.09.009CrossRefGoogle ScholarPubMed
Russell, E, Koren, G, Rieder, M and Van Uum, SH 2014 The detection of cortisol in human sweat: implications for measure-ment of cortisol in hair. Therapeutic Drug Monitoring 36: 3034CrossRefGoogle Scholar
Salaberger, T, Millard, M, Makarem, SE, Möstl, E, Grünberger, V, Krametter-Frötscher, R, Wittek, T and Palme, R 2016 Influence of external factors on hair cortisol con-centrations. General and Comparative Endocrinology 233: 7378. https://doi.org/10.1016/j.ygcen.2016.05.005CrossRefGoogle Scholar
Sevi, A 2009 Animal-based measures for welfare assessment. Italian Journal of Animal Science 8: 897899. https://doi.org/10.4081/ijas.2009.s2.904CrossRefGoogle Scholar
Sharpley, CF, Kauter, KG and McFarlane, JR 2009 An initial exploration of in vivo hair cortisol responses to a brief pain stres-sor: latency, localization and independence effects. Physiological Research 58: 757761CrossRefGoogle ScholarPubMed
Sharpley, CF, Kauter, KG and McFarlane, JR 2010 Hair cor-tisol concentration differs across site and person: localization and consistency of responses to a brief pain stressor. Physiological Research 59: 979983CrossRefGoogle ScholarPubMed
Slominski, A 2005 Neuroendocrine system of the skin. Dermatology 211: 199208. https://doi.org/10.1159/000087012CrossRefGoogle ScholarPubMed
Slominski, A and Mihm, MC 1996 Potential mechanism of skin response to stress. International Journal of Dermatology 35: 849851. https://doi.org/10.1111/j.1365-4362.1996.tb05049.xCrossRefGoogle ScholarPubMed
Slominski, A and Wortsman, J 2000 Neuroendocrinology of the skin. Endocrine Reviews 21: 457487. https://doi.org/10.1210/er.21.5.457Google ScholarPubMed
Slominski, A, Wortsman, J, Tuckey, RC and Paus, R 2007 Differential expression of HPA axis homologue in the skin. Molecular and Cellular Endocrinology 265: 143149. https://doi.org/10.1016/j.mce.2006.12.012CrossRefGoogle Scholar
Stalder, T and Kirschbaum, C 2012 Analysis of cortisol in hair: state of the art and future directions. Brain, Behavior and Immunity 26: 10191029. https://doi.org/10.1016/j.bbi.2012.02.002CrossRefGoogle ScholarPubMed
Stubsjøen, SM, Bohlin, J, Dahl, E, Knappe-Poindecker, M, Fjeldaas, T, Lepschy, M, Palme, R, Langbein, J and Ropstad, E 2015 Assessment of chronic stress in sheep (part I): The use of cortisol and cortisone in hair as non-invasive biological markers. Small Ruminant Research 132: 2531. https://doi.org/10.1016/j.smallrumres.2015.09.015CrossRefGoogle Scholar
Szeto, A, Gonzales, JA, Spitzer, SB, Levine, JE, Zaias, J, Saab, PG, Schneiderman, N and McCabe, PM 2004 Circulating lev-els of glucocorticoid hormones in WHHL and NZW rabbits: cir-cadian cycle and response to repeated social encounter. Psychoneuroendocrinology 29: 861866. https://doi.org/10.1016/S0306-4530(03)00153-7CrossRefGoogle Scholar
Teskey-Gerstl, A, Bamberg, W, Steineck, T and Palme, R 2000 Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). Journal of Comparative Physiology. B, Biochemical, Systemic and Environmental Physiology 170: 163168. https://doi.org/10.1007/s003600050271CrossRefGoogle ScholarPubMed
Thomson, S, Koren, G, Fraser, LA, Rieder, M, Friedman, TC and Van Uum, SH 2010 Hair analysis provides a historical record of cortisol levels in Cushing's syndrome. Experimental and Clinical Endocrinology & Diabetes: Official Journal, German Society of Endocrinology and German Diabetes Association 118: 133138. https://doi.org/10.1055/s-0029-1220771CrossRefGoogle ScholarPubMed
Walker, DJ, Elliott, J and Syme, HM 2009 Urinary cortisol/cor-tisone ratios in hypertensive and normotensive cats. Journal of Feline Medicine and Surgery 11: 442448. https://doi.org/10.1016/j.jfms.2008.10.004CrossRefGoogle ScholarPubMed
Zmijewski, MA and Slominski, AT 2011 Neuroendocrinology of the skin: An overview and selective analysis. Dermato-endocrinol-ogy 3(1): 310. https://doi.org/10.4161/derm.3.1.14617CrossRefGoogle ScholarPubMed