Hair cortisol; Indicator; Monitoring; Phenotype; Welfare; Animal Science and Zoology
Abstract :
[en] Stress in dairy herds can occur from multiple sources. When stress becomes chronic because of a long duration and inability of animals to adapt, it is likely to deeply affect the emotional state, health, immunity, fertility and milk production of cows. While assessing chronic stress in herds would be beneficial, no real consensus has emerged from the literature regarding the indicators of interest. The goal of this study was to compare and evaluate potential biomarkers for chronic stress after inducing stress over a 4-week period through severe overstocking, restricted access to feed and isolated unusual events. A total of 30 cows were involved in the experiment and two similar groups were constituted. Over a 4-week period, the 15 cows of the stress group were housed in overstocked conditions, with 4.6 m2 per cow, including resting and feeding areas. In this area, only seven individual places at the feeding area were available for the 15 cows to generate competition for feed access. Twice during the trial and over a period of 2 h, an additional stress was induced by moving cows to an unfamiliar barn and diffusion of stressing noises (dog barking). Meanwhile, the 15 cows of the control group stayed in the original barn, with more than 10 m2 per cow and more individual places at the feeding area than cow number. On a weekly basis, several variables considered as potential biomarkers for chronic stress were recorded. Collected data were analysed using single trait linear repeated mixed models. No differences were observed regarding milk yield, BW of cows or body condition score but the milk loss was more pronounced in the stress group. The activity was more heterogeneous and the rumination of cows was lower in the stress group. The heart rate was lower in the stress group and showed more heterogeneity at the end of the stress period. No differences were observed regarding salivary cortisol, blood glucose, β-endorphin, thyroxine and leucocyte profile. A higher level of hair cortisol and blood fructosamine were observed in the stress group at the end of the stress period. Regarding the practical use of the highlighted biomarkers, milk loss may be an effective and easy way to detect general problems, including stress. The blood fructosamine and the hair cortisol concentrations are promising indicators to assess chronic stress in commercial farms.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Grelet, C; Walloon Agricultural Research Center (CRA-W), 5030 Gembloux, Belgium
Vanden Dries, V; Walloon Agricultural Research Center (CRA-W), 5030 Gembloux, Belgium
Leblois, Julie ; Université de Liège - ULiège > TERRA Research Centre > Ingénierie des productions animales et nutrition ; Elevéo asbl by awé groupe, 5590 Ciney, Belgium
Wavreille, José ; Université de Liège - ULiège > Département GxABT
Mirabito, L; French Livestock Institute (IDELE), 75595 Paris, France
Soyeurt, Hélène ; Université de Liège - ULiège > Département GxABT
The authors gratefully thank Fran?ois Rouelle, Maxence Didelez, Sophie Mathieux, Maxime Druez, Quentin Vigneron, Mohamed El Morabit, Matthieu Dubuisson, Octave Christophe, Petimat Kitaeva & Olivier Genard for their highly valuable work. The authors also acknowledge Virginie Decruyenaere, Eric Froidmont and Pierre Rondia for their help. Preprint reference: 10.21203/rs.3.rs-569271/v1. HappyMoo project and the CRA-W acknowledge INTERREG NWE (grant agreement n? NWE730) and the Walloon Region for their financial support.HappyMoo project and the CRA-W acknowledge INTERREG NWE (grant agreement n° NWE730) and the Walloon Region for their financial support.
Abdelkrim, A.B., Puillet, L., Gomes, P., Martin, O., Lactation curve model with explicit representation of perturbations as a phenotyping tool for dairy livestock precision farming. Animal, 15, 2021, 100074.
Adriaens, I., Huybrechts, T., Aernouts, B., Geerinckx, K., Piepers, S., De Ketelaere, B., Saeys, W., Method for short-term prediction of milk yield at the quarter level to improve udder health monitoring. Journal of Dairy Science 101 (2018), 10327–10336.
do Amaral, B.C., Connor, E.E., Tao, S., Hayen, M.J., Bubolz, J.W., Dahl, G.E., Heat stress abatement during the dry period influences metabolic gene expression and improves immune status in the transition period of dairy cows. Journal of Dairy Science 94 (2011), 86–96.
Bjerre-Harpøth, V., Friggens, N.C., Thorup, V.M., Larsen, T., Damgaard, B.M., Ingvartsen, K.L., Moyes, K.M., Metabolic and production profiles of dairy cows in response to decreased nutrient density to increase physiological imbalance at different stages of lactation. Journal of Dairy Science 95 (2012), 2362–2380.
von Borell, E., Dobson, H., Prunier, A., Stress, behaviour and reproductive performance in female cattle and pigs. Hormones and Behavior 52 (2007), 130–138.
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., Veissier, I., Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals - a review. Physiology and Behavior 92 (2007), 293–316.
Braun, U., Clavadetscher, G., Baumgartner, M.R., Riond, B., Binz, T.M., Hair cortisol concentration and adrenal gland weight in healthy and ill cows. Schweizer Archiv fur Tierheilkunde 159 (2017), 493–495.
Brito, L.F., Oliveira, H.R., McConn, B.R., Schinckel, A.P., Arrazola, A., Marchant-Forde, J.N., Johnson, J.S., Large-scale phenotyping of livestock welfare in commercial production systems: a new frontier in animal breeding. Frontiers in Genetics, 11, 2020, 793.
Burnett, T.A., Madureira, A.M.L., Silper, B.F., Nadalin, A., Tahmasbi, A., Veira, D.M., Cerri, R.L.A., Short communication: factors affecting hair cortisol concentrations in lactating dairy cows. Journal of Dairy Science 97 (2014), 7685–7690.
Burnett, T.A., Madureira, A.M.L., Silper, B.F., Tahmasbi, A., Nadalin, A., Veira, D.M., Cerri, R.L.A., Relationship of concentrations of cortisol in hair with health, biomarkers in blood, and reproductive status in dairy cows. Journal of Dairy Science 98 (2015), 4414–4426.
Caré, S., Trevisi, E., Minuti, A., Ferrari, A., Loor, J.J., Calamari, L., Plasma fructosamine during the transition period and its relationship with energy metabolism and inflammation biomarkers in dairy cows. Livestock Science 216 (2018), 138–147.
Comin, A., Peric, T., Corazzin, M., Veronesi, M.C., Meloni, T., Zufferli, V., Cornacchia, G., Prandi, A., Hair cortisol as a marker of hypothalamic-pituitary-adrenal axis activation in Friesian dairy cows clinically or physiologically compromised. Livestock Science 152 (2013), 36–41.
Comin, A., Prandi, A., Peric, T., Corazzin, M., Dovier, S., Bovolenta, S., Hair cortisol levels in dairy cows from winter housing to summer highland grazing. Livestock Science 138 (2011), 69–73.
Cook, N.B., Mentink, R.L., Bennett, T.B., Burgi, K., The effect of heat stress and lameness on time budgets of lactating dairy cows. Journal of Dairy Science 90 (2007), 1674–1682.
Dobson, H., Smith, R.F., What is stress, and how does it affect reproduction?. Animal Reproduction Science 60 (2000), 743–752.
Elsasser, T.H., Steele, N.C., Fayer, R., Cytokines, Stress, and Growth Modulation. Myers, M.J., Murtaugh, M.P., (eds.) Cytokines in Animal Health and Disease, 2020, CRC Press, Boca Raton, FL, USA, 261–290.
Ferguson, J.D., Galligan, D.T., Thomsen, N., Principal Descriptors of Body Condition Score in Holstein Cows. Journal of Dairy Science 77 (1994), 2695–2703.
Fink, G., Stress: Definition and history. Squire, L.R., (eds.) Encyclopedia of Neuroscience, 2009, Academic Press, San Diego, CA, USA, 549–555.
Fischer-Tenhagen, C., Ladwig-Wiegard, M., Heuwieser, W., Thöne-Reineke, C., Short communication: is hair cortisol a potential indicator for stress caused by chronic lameness in dairy cows?. Journal of Dairy Science 101 (2018), 5439–5443.
Fisher, A.D., Crowe, M.A., Prendiville, D.J., Enright, W.J., Indoor space allowance: effects on growth, behaviour, adrenal and immune responses of finishing beef heifers. Animal Science 64 (1997), 53–62.
Friend, T.H., Dellmeier, G.R., Gbur, E.E., Comparison of four methods of calf confinement. I. Physiology. Journal of animal Science 60 (1985), 1095–1101.
Fustini, M., Galeati, G., Gabai, G., Mammi, L.E., Bucci, D., Baratta, M., Accorsi, P.A., Formigoni, A., Overstocking dairy cows during the dry period affects dehydroepiandrosterone and cortisol secretion. Journal of Dairy Science 100 (2017), 620–628.
González-de-la-Vara, M. del R., Valdez, R.A., Lemus-Ramirez, V., Vázquez-Chagoyán, J.C., Villa-Godoy, A., Romano, M.C., Effects of adrenocorticotropic hormone challenge and age on hair cortisol concentrations in dairy cattle. Canadian Journal of Veterinary Research 75 (2011), 216–221.
Heimbürge, S., Kanitz, E., Otten, W., The use of hair cortisol for the assessment of stress in animals. General and Comparative Endocrinology 270 (2019), 10–17.
Heimbürge, S., Kanitz, E., Tuchscherer, A., Otten, W., Within a hair's breadth – factors influencing hair cortisol levels in pigs and cattle. General and Comparative Endocrinology, 288, 2020, 113359.
Heimbürge, S., Kanitz, E., Tuchscherer, A., Otten, W., Is it getting in the hair? – Cortisol concentrations in native, regrown and segmented hairs of cattle and pigs after repeated ACTH administrations. General and Comparative Endocrinology, 295, 2020, 113534.
Herskin, M.S., Munksgaard, L., Ladewig, J., Effects of acute stressors on nociception, adrenocortical responses and behavior of dairy cows. Physiology & Behavior 83 (2004), 411–420.
Ito, N., Ito, T., Kromminga, A., Bettermann, A., Takigawa, M., Kees, F., Straub, R.H., Paus, R., Human hair follicles display a functional equivalent of the hypothalamic-pituitary-adrenal (HPA) axis and synthesize cortisol. The FASEB Journal 19 (2005), 1332–1334.
Jain, N.C., Essentials of veterinary hematology. 1993, Lea and Febiger, Philadelphia, PA, USA.
Jensen, A.L., Petersen, M.B., Houe, H., Determination of the Fructosamine Concentration in Bovine Serum Samples. Journal of Veterinary Medicine Series A 40 (1993), 111–117.
Ketelaar-De Lauwere, C.C., Devir, S., Metz, J.H.M., The influence of social hierarchy on the time budget of cows and their visits to an automatic milking system. Applied Animal Behaviour Science 49 (1996), 199–211.
Kovács, L., Kézér, F.L., Jurkovich, V., Kulcsár-Huszenicza, M., Tözsér, J., Hillmann, E., Heart rate variability as an indicator of chronic stress caused by lameness in dairy cows. PLoS ONE, 10, 2015, e0134792.
Kovács, L., Kézér, F.L., Ruff, F., Szenci, O., Rumination time and reticuloruminal temperature as possible predictors of dystocia in dairy cows. Journal of Dairy Science 100 (2017), 1568–1579.
Lacetera, N., Bernabucci, U., Scalla, D., Basirico, L., Morera, P., Nardone, A., Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. Journal of Dairy Science 89 (2006), 4606–4612.
Meyer, J.S., Novak, M.A., Minireview: Hair cortisol: A novel biomarker of hypothalamic-pituitary- adrenocortical activity. Endocrinology 153 (2012), 4120–4127.
Min, L., Zheng, N., Zhao, S., Cheng, J., Yang, Y., Zhang, Y., Yang, H., Wang, J., Long-term heat stress induces the inflammatory response in dairy cows revealed by plasma proteome analysis. Biochemical and Biophysical Research Communications 471 (2016), 296–302.
Moberg, G.P., Anderson, C.O., Underwood, T.R., Ontogeny of the adrenal and behavioral responses of lambs to emotional stress. Journal of Animal Science 51 (1980), 138–142.
Mohr, E., Langbein, J., Nürnberg, G., Heart rate variability: A noninvasive approach to measure stress in calves and cows. Physiology and Behavior 75 (2002), 251–259.
Mormède, P., Andanson, S., Aupérin, B., Beerda, B., Guémené, D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C.G., Richard, S., Veissier, I., Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology and Behavior 92 (2007), 317–339.
Moya, D., Schwartzkopf-Genswein, K.S., Veira, D.M., Standardization of a non-invasive methodology to measure cortisol in hair of beef cattle. Livestock Science 158 (2013), 138–144.
Müschner-Siemens, T., Hoffmann, G., Ammon, C., Amon, T., Daily rumination time of lactating dairy cows under heat stress conditions. Journal of Thermal Biology, 88, 2020, 102484.
Nedić, S., Pantelić, M., Vranješ-Durić, S., Nedić, D., Jovanović, L., Cebulj-Kadunc, N., Kobal, S., Snoj, T., Kirovski, D., Cortisol concentrations in hair, blood and milk of Holstein and Busha cattle. Slovenian Veterinary Research 54 (2017), 163–172.
Peric, T., Comin, A., Corazzin, M., Montillo, M., Cappa, A., Campanile, G., Prandi, A., Short communication: hair cortisol concentrations in Holstein-Friesian and crossbreed F1 heifers. Journal of Dairy Science 96 (2013), 3023–3027.
Poppe, M., Veerkamp, R.F., van Pelt, M.L., Mulder, H.A., Exploration of variance, autocorrelation, and skewness of deviations from lactation curves as resilience indicators for breeding. Journal of Dairy Science 103 (2020), 1667–1684.
Proudfoot, K.L., Weary, D.M., LeBlanc, S.J., Mamedova, L.K., von Keyserlingk, M.A.G., Exposure to an unpredictable and competitive social environment affects behavior and health of transition dairy cows. Journal of Dairy Science 101 (2018), 9309–9320.
Roland, L., Drillich, M., Fidlschuster, B., Schwendenwein, I., Iwersen, M., Short communication: Evaluation of an automated in-house hematology analyzer for bovine blood. Journal of Dairy Science 97 (2014), 5580–5586.
Romero, L.M., Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution 19 (2004), 249–255.
Rosner, B., Fundamentals of biostatistics. 2011, Brooks & Cole Cengage Learning, Boston, MA, USA.
Safa, S., Kargar, S., Moghaddam, G.A., Ciliberti, M.G., Caroprese, M., Heat stress abatement during the postpartum period: effects on whole lactation milk yield, indicators of metabolic status, inflammatory cytokines, and biomarkers of the oxidative stress. Journal of Animal Science 97 (2019), 122–132.
Salak-Johnson, J.L., McGlone, J.J., Making sense of apparently conflicting data: stress and immunity in swine and cattle. Journal of animal science 85 (2007), E81–E88.
Schubach, K.M., Cooke, R.F., Brandão, A.P., Lippolis, K.D., Silva, L.G.T., Marques, R.S., Bohnert, D.W., Impacts of stocking density on development and puberty attainment of replacement beef heifers. Animal 11 (2017), 2260–2267.
Schüller, L.K., Burfeind, O., Heuwieser, W., Effect of short- and long-term heat stress on the conception risk of dairy cows under natural service and artificial insemination breeding programs. Journal of Dairy Science 99 (2016), 2996–3002.
Schwinn, A.C., Knight, C.H., Bruckmaier, R.M., Gross, J.J., Suitability of saliva cortisol as a biomarker for hypothalamic–pituitary–adrenal axis activation assessment, effects of feeding actions, and immunostimulatory challenges in dairy cows. Journal of Animal Science 94 (2016), 2357–2365.
Selye, H., A syndrome produced by diverse nocuous agents. Nature, 138, 1936, 32.
Selye, H., Stress without Distress. 1976, Springer, Boston, MA, USA, 137–147.
Steinhoff, L., Jung, K., Meyerholz, M.M., Heidekorn-Dettmer, J., Hoedemaker, M., Schmicke, M., Thyroid hormone profiles and TSH evaluation during early pregnancy and the transition period in dairy cows. Theriogenology 129 (2019), 23–28.
Tallo-Parra, O., Albanell, E., Carbajal, A., Monclús, L., Manteca, X., Lopez-Bejar, M., Prediction of Cortisol and Progesterone Concentrations in Cow Hair Using Near-Infrared Reflectance Spectroscopy (NIRS). Applied Spectroscopy 71 (2017), 1954–1961.
Tallo-Parra, O., Carbajal, A., Monclús, L., Manteca, X., Lopez-Bejar, M., Hair cortisol and progesterone detection in dairy cattle: interrelation with physiological status and milk production. Domestic Animal Endocrinology 64 (2018), 1–8.
Tallo-Parra, O., Lopez-Bejar, M., Carbajal, A., Monclús, L., Manteca, X., Devant, M., Acute ACTH-induced elevations of circulating cortisol do not affect hair cortisol concentrations in calves. General and Comparative Endocrinology 240 (2017), 138–142.
Tallo-Parra, O., Manteca, X., Sabes-Alsina, M., Carbajal, A., Lopez-Bejar, M., Hair cortisol detection in dairy cattle by using EIA: Protocol validation and correlation with faecal cortisol metabolites. Animal 9 (2015), 1059–1064.
Trevisi, E., Bertoni, G., Some physiological and biochemical methods for acute and chronic stress evaluation in dairy cows. Italian Journal of Animal Science 8 (2009), 265–286.
Udo, H.M.J., Hair coat characteristics in Friesian heifers in the Netherlands and Kenya: experimental data and a review of literature. 1978, Wageningen University and Research, Wageningen, The Netherlands.
Vesel, U., Pavič, T., Ježek, J., Snoj, T., Starič, J., Welfare assessment in dairy cows using hair cortisol as a part of monitoring protocols. Journal of Dairy Research 87 (2020), 72–78.
Waiblinger, S., Menke, C., Coleman, G., The relationship between attitudes, personal characteristics and behaviour of stockpeople and subsequent behaviour and production of dairy cows. Applied Animal Behaviour Science 79 (2002), 195–219.
Walker, S.L., Smith, R.F., Jones, D.N., Routly, J.E., Dobson, H., Chronic stress, hormone profiles and estrus intensity in dairy cattle. Hormones and Behavior 53 (2008), 493–501.
Quality, W., Welfare Quality® Assessment Protocol for Cattle, 1–142. 2009, Welfare Quality R Consortium, Lelystad, The Netherlands.
Westgard, S., Petrides, V., Schneider, S., Berman, M., Herzogenrath, J., Orzechowski, A., Assessing precision, bias and sigma-metrics of 53 measurands of the Alinity ci system. Clinical Biochemistry 50 (2017), 1216–1221.