Steroids in pig hair and welfare evaluation systems: combined approaches to improve management in pig breeding?
DOI:
https://doi.org/10.12834/VetIt.1974.11885.1Keywords:
Cortisol, CReNBA, Dehydroepiandrosterone-sulphate, Hair, SwineAbstract
The aim of the present pilot study was to determine the allostatic load by analysing the hair cortisol and dehydroepiandrosterone‑sulphate (DHEA‑S) of commercial pigs belonging to different farms having good overall animal welfare according to the CREnBA (Centro di Referenza Nazionale per il Benessere Animale – Brescia, Italy) assessment protocol. The study was conducted on 86 pigs belonging to three farms with a grade higher than 8 on the CReNBA welfare evaluation system. Hair samples were taken by shaving on sows 1‑10 days after weaning (Farms 1 and 2) and at the age of 8‑10 months (Farm 3). The hormone concentrations were measured by radioimmunoassay. From the box plots, it is evident that the hair cortisol concentrations of animals were different between farms. Conversely, the variability of the hair DHEA‑S concentration was similar between the F1 and F2 farms but much lower at F3. For all the variables considered (cortisol, DHEA‑S and cortisol/DHEA‑S ratio), F2 showed a higher hair concentration level than F1 (P < 0.05). The study’s results indicate that the measurement of cortisol and DHEA‑S in pig hair shows a different allostatic load between them, although the official welfare evaluation method assessed the farms as having good overall animal welfare.
References
Ali O.S., Badawy N., Rizk S., Gomaa H. & Saleh M.S. 2016. Allostatic Load Assessment for Early Detection of Stress in the Workplace in Egypt. Open Access Maced. J Med Sci, 15, 493-498.
Antonides A., Schoonderwoerd A.C., Nordquist R.E. & van der Staay F.J. 2015. Very low birth weight piglets show improved cognitive performance in the spatial cognitive holeboard task. Front Behav Neurosci, 9, 43.
Bacci M.L., Nannoni E., Govoni N., Scorrano F., Zannoni A., Forni M., Martelli G. & Sardi L. 2014. Hair cortisol determination in sows in two consecutive reproductive cycles. Reprod Biol, 14, 218-223.
Bacou E., Haurogné K., Mignot G., Allard M., De Beaurepaire L., Marchand J., Terenina E., Billon Y., Jacques J., Bach J.M., Mormède P., Hervé J. & Lieubeau B. 2017. Acute social stress-induced immunomodulation in pigs high and low responders to ACTH. Physiol Behav, 169, 1-8.
Bergamin C., Comin A., Corazzin M., Faustini M., Peric T., Scollo A., Gottardo F., Montillo M. & Prandi A. 2019. Cortisol, DHEA, and Sexual Steroid Concentrations in Fattening Pigs' Hair. Animals (Basel), 9, E345.
Bertocchi L., Fusi F., Angelucci A., Bolzoni L., Pongolini S., Strano R.M., Ginestreti J., Riuzzi G., Moroni P. & Lorenzi V. 2018. Characterization of hazards, welfare promoters and animal-based measures for the welfare assessment of dairy cows: Elicitation of expert opinion. Prev Vet Med, 150, 8-18.
Buckham Sporer K.R., Weber P.S.D., Burton J.L., Earley B. & Crowe M.A. 2008. Transportation of young beef bulls alters circulating physiological parameters that may be effective biomarkers of stress. J Anim Sci, 86, 1325-1334.
Carroll G.A., Boyle L.A., Hanlon A., Palmer M.A., Collins L., Griffin K., Armstrong D. & O'Connell N.E. 2018. Identifying physiological measures of lifetime welfare status in pigs: exploring the usefulness of haptoglobin, C- reactive protein and hair cortisol sampled at the time of slaughter. Ir Vet J, 71, 8.
Casal N., Manteca X., Peña R., Bassols A. & Fàbrega E. 2017. Analysis of cortisol in hair samples as an indicator of stress in pigs. J Vet Behav, 19, 1-6.
Caslini C., Comin A., Peric T., Prandi A., Pedrotti L. & Mattiello S. 2016. Use of hair cortisol analysis for comparing population status in wild red deer (Cervus elaphus) living in areas with different characteristics. Eur J Wildl Res, 62, 713-723.
Cattet M., Stenhouse G.B., Janz D.M., Kapronczai L., Anne Erlenbach J., Jansen H.T., Nelson O.L., Robbins C.T. & Boulanger J. 2017. The quantification of reproductive hormones in the hair of captive adult brown bears and their application as indicators of sex and reproductive state. Conserv Physiol, 5, cox032.
Charney D.S. 2004. Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptations to extreme stress. Am. J. Psychiatry, 161, 195-216.
Comin A., Peric T., Corazzin M., Veronesi M.C., Meloni T., Zufferli V., Cornacchia G. & Prandi A. 2013. Hair cortisol as a marker of hypothalamic-pituitary-adrenal axis activation in Friesian dairy cows clinically or physiologically compromised. Livest Sci, 152, 36-41.
Comin A., Veronesi M.C., Montillo M., Faustini M., Valentini S., Cairoli F. & Prandi A. 2012. Hair cortisol level as a retrospective marker of hypothalamic-pituitary-adrenal axis activity in horse foals. Vet J, 194, 131-132.
Cooper T.A., Roberts M.P., Kattesh H.G. & Kojima C.J. 2009. Effects of transport stress, sex, and weaning weight on postweaning performance in pigs. Profess Anim Sci, 25, 189-194.
Davenport M.D., Tiefenbacher S., Lutz C.K., Novak M.A. & Meyer J.S. 2006. Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen Comp Endocrinol, 147, 255-261.
Dettmer A.M., Rosenberg K.L., Suomi S.J., Meyer J.S. & Novak M.A. 2015. Associations between Parity, Hair Hormone Profiles during Pregnancy and Lactation, and Infant Development in Rhesus Monkeys (Macaca mulatta). PLoS One, 14, e0131692.
EFSA. 2012. Scientific Opinion on the use of animal-based measures to assess welfare in pigs. EFSA J, 10, 2512.
Gallagher P., Leitch M.M., Massey A.E., McAllister-Williams R.H. & Young A.H. 2006. Assessing cortisol and dehydroepiandrosterone (DHEA) in saliva: effects of collection method. J Psychopharmacol, 20, 643-649.
Goodyer I.M., Herbert J. & Altham P.M. 1998. Adrenal steroid secretion and major depression in 8- to 16-year-olds, III. Influence of cortisol/DHEA ratio at presentation on subsequent rates of disappointing life events and persistent major depression. Psychol Med, 28, 265-273.
Grass J., Kirschbaum C., Miller R., Gao W., Steudte-Schmiedgen S. & Stalder T. 2015. Sweat-inducing physiological challenges do not result in acute changes in hair cortisol concentrations. Psychoneuroendocrinology, 53, 108-116.
Guilliams T.G. & Edwards L. 2010. Chronic stress and the HPA axis: Clinical assessment and therapeutic considerations. Standard, 9, 1-12.
Hechter O., Grossman A. & Chatterton R.T. Jr. 1997. Relationship of dehydroepiandrosterone and cortisol in disease. Med Hypotheses, 49, 85-91.
Heimbürge S., Kanitz E. & Otten W. 2019. The use of hair cortisol for the assessment of stress in animals. Gen Comp Endocrinol, 270, 10-17.
Hillmann E., Schrader L., Mayer C. & Gygax L. 2008. Effects of weight, temperature and behaviour on the circadian rhythm of salivary cortisol in growing pigs. Animal, 2, 405-409.
Kalimi M., Shafagoj Y., Loria R., Padgett D. & Regelson W. 1994. Anti-glucocorticoid effects of dehydroepiandrosterone (DHEA). Mol Cell Biochem, 131, 99-104.
Knap P. 2005. Breeding robust pigs. Austr J Experim Agric, 45, 1-11.
Kroboth P.D., Salek F.S., Pittenger A.L., Fabian T.J. & Frye R.F. 1999. DHEA and DHEA-S: A review. J Clin Pharmacol, 39, 327-348.
Labrie F., Luu-The V., Martel C., Chernomoretz A., Calvo E., Morissette J. & Labrie C. 2006. Dehydroepiandrosterone (DHEA) is an anabolic steroid like dihydrotestosterone (DHT), the most potent natural androgen, and tetrahydrogestrinone (THG). J Steroid Biochem Mol Biol, 100, 52-58.
Lee D.Y., Kim E. & Choi M.H. 2015. Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Rep, 48, 209-216.
Maninger N., Capitanio J.P., Mason W.A., Ruys J.D. & Mendoza S.P. 2010. Acute and chronic stress increase DHEAS concentrations in rhesus monkeys. Psychoneuroendocrinology, 35, 1055-1062.
Maninger N., Wolkowitz O.M., Reus V.I., Epel E.S. & Mellon S.H. 2009. Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS). Front Neuroendocrinol, 30, 65-91.
Marieb E.N. & Hoehn K. 2010. Human Anatomy & Physiology. San Francisco, California, Pearson Benjamin Cummings, 9th ed., 1264 pp.
Martelli G., Sardi L., Stancampiano L., Govoni N., Zannoni A., Nannoni E., Forni M. & Bacci M.L. 2014. A study on some welfare-related parameters of hDAF transgenic pigs when compared with their conventional close relatives. Animal, 8, 810-816.
McEwen B.S. 2003. Interacting mediators of allostasis and allostatic load: Towards an understanding of resilience in aging. Metabolism, 52, 10-16.
McEwen B.S & Wingfield J.C. 2003. The concept of allostasis in biology and biomedicine. Horm Behav, 43, 2-15.
Montillo M., Caslini C., Peric T., Prandi A., Netto P., Tubaro F., Pedrotti L., Bianchi A. & Mattiello S. 2019. Analysis of 19 Minerals and Cortisol in Red Deer Hair in Two Different Areas of the Stelvio National Park: A Preliminary Study. Animals (Basel), 9, E492.
Mormède P., Terenina E. 2012. Molecular genetics of the adrenocortical axis and breeding for robustness. Domest Anim Endocrinol, 43, 116-131.
Möstl E., Messmann E., Bagu E., Robia C. & Palme R. 1999. Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Zentralbl Veterinarmed A, 46, 621-631.
Mowafy M. & Cassens R. G. 1976. Hair growth in the domestic pig. Quantitative aspects. J Am Leather Chem Assoc, 71, 71-78.
Nielsen B.H., Angelucci A., Scalvenzi A., Forkman B., Fusi F., Tuyttens F., Houe H., Blokhuis H., Sørensen JT., Rothmann J., Matthews L., Mounier L., Bertocchi L., Richard M., Donati M., Nielsen P.P., Salinim R. deGraafm S., Hildm S. Messorim S., Nielsenm S.S., Lorenzi V., Boivin X. & Thomsen P.T. 2014. External Scientific Report on the Use of Animal Based Measures for the Assessment of Dairy Cow Welfare. EFSA supporting publication, EN-659.
Nieschlag E., Loriaux D.L., Ruder H.J., Zucker J.R., Kirschner M.A. & Lipsett M.B. 1973. The secretion of dehydroepiandrosterone and dehydroepiandrosterone sulphate in man. J Endocrinol, 57, 123-134.
Peric T., Comin A., Corazzin M., Montillo M., Canavese F., Stebel M. & Prandi A. 2017. Relocation and Hair Cortisol Concentrations in New Zealand White Rabbits. J Appl Anim Welf Sci, 20, 1-8.
Peric T., Comin A., Corazzin M., Montillo M., Cappa A., Campanile G. & Prandi A. 2013. Short communication: hair cortisol concentrations in Holstein-Friesian and crossbreed F1 heifers. J. Dairy Sci, 96, 3023-3027.
Peric T., Corazzin M., Romanzin A., Bovolenta S., Prandi A., Montillo M. & Comin A. 2017. Cortisol and DHEA concentrations in the hair of dairy cows managed indoor or on pasture. Livest Sci, 202, 39-43.
Pol F., Courboulay V., Cotte J.P., Martrenchar A., Hay M. & Mormède P. 2002. Urinary cortisol as an additional tool to assess the welfare of pregnant sows kept in two types of housing. Vet Res, 33, 13-22.
Qiao S., Li X., Zilioli S., Chen Z., Deng H., Pan J. & Guo W. 2017. Hair measurements of cortisol, DHEA, and DHEA to cortisol ratio as biomarkers of chronic stress among people living with HIV in China: Known-group validation. PLoS ONE, 12, e0169827.
RCoreTeam. 2017. (Computer software). R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. Available online: https://www.R-project.org (accessed on 13 April 2019).
Russo S.J., Murrough J.W., Han M., Charney D.S. & Nestler E.J. 2012. Neurobiology of resilience. Nat Neurosci, 15, 1475-1484.
Saczawa M.E., Graber J.A., Brooks-Gunn J. & Warren M.P. 2013. Methodological considerations in use of the cortisol/DHEA(S) ratio in adolescent populations. Psychoneuroendocrinology, 38, 2815-2819.
Skarlandtová H., Bičíková M., Neužil P., Mlček M., Hrachovina V., Svoboda T., Medová E., Kudlička J., Dohnalová A., Havránek Š., Kazihnítková H., Máčová L., Vařejková E. & Kittnar O. 2014. Are there any differences between stress hormone levels in non-stress conditions and in potentional stress overload (heart catheterisation) in sows? Physiol Res, 63, 733-741.
SPSS® Statistical package for social science SPSS. 1989-1997. (Computer software). Advanced Statistics 7.5. Chicago, IL, USA, SPSS Inc.
Stalder T. & Kirschbaum C. 2012. Analysis of cortisol in hair: State of the art and future directions. Brain Behav Immun, 26, 1019-1029.
Stradaioli G., Peric T., Montillo M., Comin A., Corazzin M., Veronesi M.C. & Prandi A. 2017. Hair cortisol and testosterone concentrations and semen production of Bos taurus bulls. Ital J Anim Sci, 16, 631-639.
Tagliaferro A.R. & Ronan A.M. 2001. Physiological levels and action of dehydroepiandrosterone in Yucatan miniature swine. Am J Physiol Regul Integr Comp Physiol, 281, R1-R9.
Thom E. 2016. Stress and the Hair Growth Cycle: Cortisol-Induced Hair Growth Disruption. J Drugs Dermatol, 15, 1001-1004.
Trevisan C., Montillo M., Prandi A., Mkupasi E.M., Ngowi H.A. & Johansen M.V. 2017. Hair cortisol and dehydroepiandrosterone concentrations in naturally Taenia solium infected pigs in Tanzania. Gen Comp Endocrinol, 246, 23-28.
Watson S.A. & Moore G.P. 1990. Postnatal development of the hair cycle in the domestic pig. J Anat, 170, 1-9.
Weary D.M., Pajor E.A., Bonenfant M., Fraser D. & Kramer D.L. 2002. Alternative housing for sows and litters: Part 4. Effects of sow-controlled housing combined with a communal piglet area on pre- and post-weaning behaviour and performance. Appl Anim Behav Sci, 76, 279-290.
Wolkowitz O.M., Epel E.S. & Reus V.I. 2001. Stress hormone-related psychopathology: pathophysiological and treatment implications. World J Biol Psychiatry, 2, 115-143.
