Identification of chronic stress biomarkers in dairy cows

Grelet, C.; Vanden Dries, V.; Leblois, J.; Wavreille, J.; Mirabito, L.; Soyeurt, H.; Franceschini, S.; Gengler, N.; Brostaux, Y.; HappyMoo Consortium; Dehareng, F.

doi:10.1016/j.animal.2022.100502

Cited by 55Animal Behavior and Welfare StudiesEffects of Environmental Stressors on LivestockAnimal health and immunology

Identification of chronic stress biomarkers in dairy cows

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Grelet, C., Vanden Dries, V., Leblois, J., Wavreille, J., Mirabito, L., Soyeurt, H., Franceschini, S., Gengler, N. +3 more·2022·animal

DOI 10.1016/j.animal.2022.100502

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Abstract

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.

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Chronic stress in dairy cows, induced by overcrowding and exposure to stressful noises, led to decreased milk production, altered activity, and increased physiological stress markers.
“Chronic stress in dairy cows, induced by overcrowding and exposure to stressful noises, led to decreased milk production, altered activity, and increased physiological stress markers.”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [120]
Bovine respiratory disease complex in beef cattle is triggered by physical, biological, and psychological stressors.
“Similarly, bovine respiratory disease complex in beef cattle is triggered by physical, biological, and psychological stressors, illustrating the economic and health impacts of stress in livestock [119,120].”
From Comprehensive review of chronic stress pathways and the efficacy of behavioral stress reduction programs (BSRPs) in managing diseases. (2024) · cites this paper as [120]

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A Syndrome produced by Diverse Nocuous Agents
Selye, H. (1936) · Nature · doi:10.1038/138032a0 · Cited by 3,967 · see citing works
Principal Descriptors of Body Condition Score in Holstein Cows
Ferguson, J. D., Galligan, D. T., & Thomsen, N. K. (1994) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(94)77212-x · Cited by 1,540 · see citing works
Physiological stress in ecology: lessons from biomedical research
Romero, L. M. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.03.008 · Cited by 1,440 · see citing works
Essentials of Veterinary Hematology
Jain, N. C. (1993) · Cited by 1,345 · see citing works
Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals — A review
von Borell, E., Langbein, J., Desprès, G., Hansen, S., Leterrier, C., Marchant, J. N., Marchant-Forde, R. M., Minero, M., Möhr, E., Prunier, A., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.01.007 · Cited by 973 · see citing works
Encyclopedia of Neuroscience
(2009) · doi:10.1007/978-3-540-29678-2 · Cited by 900 · see citing works
Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare
Mormède, P., Andanson, S., Aupérin, B., Beerda, B., Guemene, D. D., Malmkvist, J., Manteca, X., Manteuffel, G., Prunet, P., van Reenen, C. G., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.12.003 · Cited by 821 · see citing works
Assessing the human–animal relationship in farmed species: A critical review
Waiblinger, S., Boivin, X., Pedersen, V., Tosi, M.-V., Janczak, A. M., Visser, E. K., & Jones, R. B. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.02.001 · Cited by 751 · see citing works
Fundamentals of Biostatistics
Rao, K. J. P. H., Janardhan, K., & Rao, P. (2010) · Cited by 559 · see citing works
What is stress, and how does it affect reproduction?
Dobson, H., & Smith, R. F. (2000) · Animal Reproduction Science · doi:10.1016/s0378-4320(00)00080-4 · Cited by 549 · see citing works
Human hair follicles display a functional equivalent of the hypothalamic‐pituitary‐adrenal (HPA) axis and synthesize cortisol
Ito, N., Ito, T., Kromminga, A., Bettermann, A., Takigawa, M., Kees, F., Straub, R. H., & Paus, R. (2005) · The FASEB Journal · doi:10.1096/fj.04-1968fje · Cited by 498 · see citing works
Minireview: Hair cortisol: A novel biomarker of hypothalamic-pituitary-adrenocortical activity
Meyer, J. S., & Novak, M. A. (2012) · Endocrinology · doi:10.1210/en.2012-1226 · Cited by 457 · see citing works
Fructosamine: structure, analysis, and clinical usefulness.
Armbruster, D. (1987) · Clinical Chemistry · doi:10.1093/clinchem/33.12.2153 · Cited by 440 · see citing works
Stress without Distress
Selye, H. (1976) · Springer eBooks · doi:10.1007/978-1-4684-2238-2_9 · Cited by 425 · see citing works
The use of hair cortisol for the assessment of stress in animals
Heimbürge, S., Kanitz, E., & Otten, W. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.09.016 · Cited by 329 · see citing works
The relationship between attitudes, personal characteristics and behaviour of stockpeople and subsequent behaviour and production of dairy cows
Waiblinger, S., Menke, C., & Coleman, G. J. (2002) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(02)00155-7 · Cited by 292 · see citing works
The Effect of Heat Stress and Lameness on Time Budgets of Lactating Dairy Cows
Cook, N. B., Mentink, R. L., Bennett, T. B., & Burgi, K. (2007) · Journal of Dairy Science · doi:10.3168/jds.2006-634 · Cited by 277 · see citing works
Making sense of apparently conflicting data: Stress and immunity in swine and cattle1
Salak‐Johnson, J. L., & McGlone, J. J. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-538 · Cited by 255 · see citing works
Exploration of variance, autocorrelation, and skewness of deviations from lactation curves as resilience indicators for breeding
Poppe, M., Veerkamp, R. F., van Pelt, M. L., & Mulder, H. A. (2019) · Journal of Dairy Science · doi:10.3168/jds.2019-17290 · Cited by 219 · see citing works
Heart rate variability
Möhr, E., Langbein, J., & Nürnberg, G. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00651-5 · Cited by 213 · see citing works
Heat stress abatement during the dry period influences metabolic gene expression and improves immune status in the transition period of dairy cows
do Amaral, B. C., Connor, E. E., Tao, S., Hayen, M. J., Bubolz, J. W., & Dahl, G. E. (2010) · Journal of Dairy Science · doi:10.3168/jds.2009-3004 · Cited by 196 · see citing works
Heat Stress Elicits Different Responses in Peripheral Blood Mononuclear Cells from Brown Swiss and Holstein Cows
Lacetera, N., Bernabucci, U., Scalia, D., Basiricò, L., Morera, P., & Nardone, A. (2006) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(06)72510-3 · Cited by 193 · see citing works
Stress: Definition and History
Fink, G. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.00076-0 · Cited by 191 · see citing works
Large-Scale Phenotyping of Livestock Welfare in Commercial Production Systems: A New Frontier in Animal Breeding
Brito, L. F., de Oliveira, H. R., McConn, B. R., Schinckel, A. P., Arrazola, A., Marchant, J. N., & Johnson, J. S. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00793 · Cited by 173 · see citing works
Stress, behaviour and reproductive performance in female cattle and pigs
von Borell, E., Dobson, H., & Prunier, A. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.03.014 · Cited by 163 · see citing works
Heat Stress in Dairy Cattle Alters Lipid Composition of Milk
Liu, Z., Ezernieks, V., Wang, J., Arachchillage, N. W., Garner, J. B., Wales, W. J., Cocks, B. G., & Rochfort, S. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-01120-9 · Cited by 154 · see citing works
Metabolic and production profiles of dairy cows in response to decreased nutrient density to increase physiological imbalance at different stages of lactation
Bjerre-Harpøth, V., Friggens, N. C., Thorup, V. M., Larsen, T., Damgaard, B. M., Ingvartsen, K. L., & Moyes, K. M. (2012) · Journal of Dairy Science · doi:10.3168/jds.2011-4419 · Cited by 144 · see citing works
Short communication: Factors affecting hair cortisol concentrations in lactating dairy cows
Burnett, T. A., Madureira, A. M. L., Silper, B. F., Nadalin, A., Tahmasbi, A. M., Veira, D. M., & Cerri, R. L. A. (2014) · Journal of Dairy Science · doi:10.3168/jds.2014-8444 · Cited by 139 · see citing works
Standardization of a non-invasive methodology to measure cortisol in hair of beef cattle
Moya, D., Schwartzkopf-Genswein, K. S., & Veira, D. M. (2013) · Livestock Science · doi:10.1016/j.livsci.2013.10.007 · Cited by 139 · see citing works
Effects of acute stressors on nociception, adrenocortical responses and behavior of dairy cows
Herskin, M. S., Munksgaard, L., & Ladewig, J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.027 · Cited by 123 · see citing works
Comparison of Four Methods of Calf Confinement. I. Physiology2
Friend, T. H., Dellmeier, G. R., & Gbur, E. E. (1985) · Journal of Animal Science · doi:10.2527/jas1985.6051095x · Cited by 114 · see citing works
The influence of social hierarchy on the time budget of cows and their visits to an automatic milking system
Lauwere, C. C. K.-D., Devir, S., & Metz, J. H. M. (1996) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(96)01030-1 · Cited by 103 · see citing works
Relationship of concentrations of cortisol in hair with health, biomarkers in blood, and reproductive status in dairy cows
Burnett, T. A., Madureira, A. M. L., Silper, B. F., Tahmasbi, A. M., Nadalin, A., Veira, D. M., & Cerri, R. L. A. (2015) · Journal of Dairy Science · doi:10.3168/jds.2014-8871 · Cited by 101 · see citing works
Chronic stress, hormone profiles and estrus intensity in dairy cattle
Walker, S. L., Smith, R. F., Jones, D. N., Routly, J. E., & Dobson, H. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.12.003 · Cited by 100 · see citing works
Hair cortisol as a marker of hypothalamic-pituitary-adrenal axis activation in Friesian dairy cows clinically or physiologically compromised
Comin, A., Peric, T., Corazzin, M., Veronesi, M. C., Meloni, T., Zufferli, V., Cornacchia, G., & Prandi, A. (2012) · Livestock Science · doi:10.1016/j.livsci.2012.11.021 · Cited by 91 · see citing works
Hair cortisol levels in dairy cows from winter housing to summer highland grazing
Comin, A., Prandi, A., Peric, T., Corazzin, M., Dovier, S., & Bovolenta, S. (2011) · Livestock Science · doi:10.1016/j.livsci.2010.12.009 · Cited by 90 · see citing works
Within a hair’s breadth – Factors influencing hair cortisol levels in pigs and cattle
Heimbürge, S., Kanitz, E., Tuchscherer, A., & Otten, W. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113359 · Cited by 89 · see citing works
Some physiological and biochemical methods for acute and chronic stress evaluationin dairy cows
Trevisi, E., & Bertoni, G. (2009) · Italian Journal of Animal Science · doi:10.4081/ijas.2009.s1.265 · Cited by 85 · see citing works
Heart Rate Variability as an Indicator of Chronic Stress Caused by Lameness in Dairy Cows
Kovács, L., Kézér, F. L., Jurkovich, V., Kulcsár-Huszenicza, M., & Tőzsér, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134792 · Cited by 83 · see citing works
Hair cortisol detection in dairy cattle by using EIA: protocol validation and correlation with faecal cortisol metabolites
Talló-Parra, O., Manteca, X., Sabés‐Alsina, M., Carbajal, A., & López‐Béjar, M. (2015) · animal · doi:10.1017/s1751731115000294 · Cited by 83 · see citing works
Long-term heat stress induces the inflammatory response in dairy cows revealed by plasma proteome analysis
Li, M., Zheng, N., Zhao, S., Cheng, J., Yang, Y., Zhang, Y., Yang, H., & Wang, J. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.01.185 · Cited by 79 · see citing works
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
Safa, S., Kargar, S., Moghaddam, G. A., Ciliberti, M. G., & Caroprese, M. (2018) · Journal of Animal Science · doi:10.1093/jas/sky408 · Cited by 76 · see citing works
Daily rumination time of lactating dairy cows under heat stress conditions
Müschner-Siemens, T., Hoffmann, G., Ammon, C., & Amon, T. (2019) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2019.102484 · Cited by 76 · see citing works
Indoor space allowance: effects on growth, behaviour, adrenal and immune responses of finishing beef heifers
Fisher, A. D., Crowe, M. A., Prendiville, D. J., & Enright, W. J. (1997) · Animal Science · doi:10.1017/s135772980001554x · Cited by 71 · see citing works
Ontogeny of the Adrenal and Behavioral Responses of Lambs to Emotional Stress
Moberg, G. P., Anderson, C. O., & Underwood, T. R. (1980) · Journal of Animal Science · doi:10.2527/jas1980.511138x · Cited by 67 · see citing works
Cytokines in Animal Health and Disease
Myers, M. J., & Murtaugh, M. P. (2020) · CRC Press eBooks · doi:10.1201/9781003067382 · Cited by 62 · see citing works
Rumination time and reticuloruminal temperature as possible predictors of dystocia in dairy cows
Kovács, L., Kézér, F. L., Ruff, F., & Szenci, O. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-11884 · Cited by 58 · see citing works
Effect of short- and long-term heat stress on the conception risk of dairy cows under natural service and artificial insemination breeding programs
Schüller, L. K., Burfeind, O., & Heuwieser, W. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10080 · Cited by 55 · see citing works
Lactation curve model with explicit representation of perturbations as a phenotyping tool for dairy livestock precision farming
Abdelkrim, A. B., Puillet, L., Gomes, P., & Martin, O. (2020) · animal · doi:10.1016/j.animal.2020.100074 · Cited by 54 · see citing works
Short communication: Hair cortisol concentrations in Holstein-Friesian and crossbreed F1 heifers
Peric, T., Comin, A., Corazzin, M., Montillo, M., Cappa, A., Campanile, G., & Prandi, A. (2013) · Journal of Dairy Science · doi:10.3168/jds.2012-6151 · Cited by 50 · see citing works
Impacts of stocking density on development and puberty attainment of replacement beef heifers
Schubach, K. M., Cooke, R. F., Brandão, A. P., Lippolis, K. D., Silva, L. G. T., Marques, R. S., & Bohnert, D. W. (2017) · animal · doi:10.1017/s1751731117001070 · Cited by 50 · see citing works
Determination of the Fructosamine Concentration in Bovine Serum Samples
Jensen, A. L., PETERSEN, M. B., & Houe, H. (1993) · Zentralblatt für Veterinärmedizin Reihe A · doi:10.1111/j.1439-0442.1993.tb00607.x · Cited by 47 · see citing works
Assessing precision, bias and sigma-metrics of 53 measurands of the Alinity ci system
Westgard, S. A., Petrides, V., Schneider, S., Berman, M. I., Herzogenrath, J., & Orzechowski, A. (2017) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2017.09.005 · Cited by 47 · see citing works
Suitability of saliva cortisol as a biomarker for hypothalamic-pituitary-adrenal axis activation assessment, effects of feeding actions, and immunostimulatory challenges in dairy cows.
Schwinn, A.-C., Knight, C. H., Bruckmaier, R., & Gross, J. (2016) · Journal of Animal Science · doi:10.2527/jas.2015-0260 · Cited by 46 · see citing works
Overstocking dairy cows during the dry period affects dehydroepiandrosterone and cortisol secretion
Fustini, M., Galeati, G., Gabai, G., Mammi, L. M. E., Bucci, D., Baratta, M., Accorsi, P. A., & Formigoni, A. (2016) · Journal of Dairy Science · doi:10.3168/jds.2016-11293 · Cited by 45 · see citing works
Is it getting in the hair? – Cortisol concentrations in native, regrown and segmented hairs of cattle and pigs after repeated ACTH administrations
Heimbürge, S., Kanitz, E., Tuchscherer, A., & Otten, W. (2020) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2020.113534 · Cited by 42 · see citing works
Hair cortisol and progesterone detection in dairy cattle: interrelation with physiological status and milk production
Talló-Parra, O., Carbajal, A., Monclús, L., Manteca, X., & López‐Béjar, M. (2018) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2018.02.001 · Cited by 37 · see citing works
Acute ACTH-induced elevations of circulating cortisol do not affect hair cortisol concentrations in calves
Talló-Parra, O., López‐Béjar, M., Carbajal, A., Monclús, L., Manteca, X., & Devant, M. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.10.007 · Cited by 35 · see citing works
CORTISOL CONCENTRATIONS IN HAIR, BLOOD AND MILK OF HOLSTEIN AND BUSHA CATTLE
Nedić, S., Pantelić, M., Vranješ‐Đurić, S., Nedic, D. N., Jovanović, L., Čebulj-Kadunc, N., Kobal, S., Snoj, T., & Kirovski, D. (2017) · Slovenian Veterinary Research · doi:10.26873/svr-398-2017 · Cited by 34 · see citing works
Exposure to an unpredictable and competitive social environment affects behavior and health of transition dairy cows
Proudfoot, K. L., Weary, D. M., LeBlanc, S. J., Mamedova, L. K., & von Keyserlingk, M. A. G. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-14115 · Cited by 33 · see citing works
Welfare assessment in dairy cows using hair cortisol as a part of monitoring protocols
Vesel, U., Pavič, T., Ježek, J., Snoj, T., & Starič, J. (2020) · Journal of Dairy Research · doi:10.1017/s0022029920000588 · Cited by 33 · see citing works
Method for short-term prediction of milk yield at the quarter level to improve udder health monitoring
Adriaens, I., Huybrechts, T., Aernouts, B., Geerinckx, K., Piepers, S., Ketelaere, B. D., & Saeys, W. (2018) · Journal of Dairy Science · doi:10.3168/jds.2018-14696 · Cited by 24 · see citing works
Short communication: Is hair cortisol a potential indicator for stress caused by chronic lameness in dairy cows?
Fischer‐Tenhagen, C., Wiegard, M., Heuwieser, W., & Thöne‐Reineke, C. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-13967 · Cited by 23 · see citing works
Plasma fructosamine during the transition period and its relationship with energy metabolism and inflammation biomarkers in dairy cows
Carè, S., Trevisi, E., Minuti, A., Ferrari, A. R., Loor, J. J., & Calamari, L. (2018) · Livestock Science · doi:10.1016/j.livsci.2018.08.003 · Cited by 23 · see citing works
Prediction of Cortisol and Progesterone Concentrations in Cow Hair Using Near-Infrared Reflectance Spectroscopy (NIRS)
Talló-Parra, O., Albanell, E., Carbajal, A., Monclús, L., Manteca, X., & López‐Béjar, M. (2017) · Applied Spectroscopy · doi:10.1177/0003702817710295 · Cited by 21 · see citing works
Thyroid hormone profiles and TSH evaluation during early pregnancy and the transition period in dairy cows
Steinhoff, L., Jung, K., Meyerholz, M., Heidekorn-Dettmer, J., Hoedemaker, M., & Schmicke, M. (2019) · Theriogenology · doi:10.1016/j.theriogenology.2019.01.023 · Cited by 20 · see citing works
An investigation of hair cortisol as a measure of long-term stress in beef cattle: results from a castration study
Creutzinger, K. C., Stookey, J. M., Marfleet, T. W., Campbell, J., Janz, D. M., Marqués, F. J., & Seddon, Y. M. (2017) · Canadian Journal of Animal Science · doi:10.1139/cjas-2016-0206 · Cited by 20 · see citing works
Hair cortisol concentration and adrenal gland weight in healthy and ill cows
Braun, U., Clavadetscher, G., Baumgartner, M. R., Riond, B., & Binz, T. M. (2017) · Schweizer Archiv für Tierheilkunde · doi:10.17236/sat00128 · Cited by 19 · see citing works
Hair coat characteristics in Friesian heifers in the Netherlands and Kenya : experimental data and a review of literature
Udo, H. M. J. (1978) · doi:10.18174/170072 · Cited by 12 · see citing works
HISTORY AND GENERAL OUTLINE OF THE STRESS CONCEPT
(1976) · Elsevier eBooks · doi:10.1016/b978-0-407-98510-0.50009-4 · Cited by 11 · see citing works
Short communication: Evaluation of an automated in-house hematology analyzer for bovine blood
Roland, L., Drillich, M., Fidlschuster, B., Schwendenwein, I., & Iwersen, M. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7736 · Cited by 5 · see citing works

Flagged first, then by citations

1 of the 72 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

González-de-la-Vara, M. del R., Valdez, R.A., Lemus-Ramirez, V., Vázquez-Chagoyán, J.C., Villa-Godoy, A., Romano, M.C., 2011. Effects of adrenocorticotropic hormone challenge and age on hair cortisol concentrations in dairy cattle. Canadian Journal of Veterinary Research 75, 216-221.

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Papinchak, L., Paudyal, S., & Pineiro, J. (2022) · Veterinary Quarterly · doi:10.1080/01652176.2022.2119622 · Cited by 8 · see citing works
Stress detection/assement in dairy cows by the determination of cortisol in hair by near-infrared (NIR), mid-infrared (MIR) and Raman spectroscopy
Christophe, O. S., Grelet, C., Simon, H., Leblois, J., Baeten, V., & Dehareng, F. (2025) · Scientific Reports · doi:10.1038/s41598-025-12332-9 · Cited by 7 · see citing works
Self-citation
Review: Understanding cattle social behaviour in modern penned production systems with AI technology: Are we tracking welfare indicators?
Fuentes, A., Han, S., Liu, J., Park, J., Yoon, S., & Park, D. S. (2026) · animal · doi:10.1016/j.animal.2026.101788 · Cited by 7 · see citing works
Review: Exploring correctness, usefulness, and feasibility of potential physiological operational welfare indicators for farmed insects to establish research priorities.
Johnson, M., & Barrett, M. (2025) · Animal · doi:10.1016/j.animal.2025.101501 · Cited by 7 · see citing works
Effects of extrinsic factors on some rumination patterns: A review
Abeni, F. (2022) · Frontiers in Animal Science · doi:10.3389/fanim.2022.1047829 · Cited by 6 · see citing works
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Beer, H. N., Karr, L. K., Shrader, T. C., & Yates, D. T. (2023) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg4030044 · Cited by 7 · see citing works
Serum cortisol level as marker of stress in camels: relationship with immunological profile
Hussen, J., & Althagafi, H. J. (2025) · Frontiers in Veterinary Science · doi:10.3389/fvets.2025.1570564 · Cited by 5 · see citing works
Management Updates on Prepartal Stress Effects on Transition Cow and Calf Health
Nikkhah, A., & Alimirzaei, M. (2023) · World s Veterinary Journal · doi:10.54203/scil.2023.wvj27 · Cited by 5 · see citing works
Postpartum hair cortisol, dehydroepiandrosterone sulfate and their ratio in beef cows: Exploring association with parity and conception outcome
Peric, T., Veronesi, M. C., Prandi, A., Fusi, J., Faustini, M., & Probo, M. (2023) · Theriogenology · doi:10.1016/j.theriogenology.2023.11.008 · Cited by 5 · see citing works
Effect of repeated HPA axis stimulation on hair cortisol concentration, growth, and behavior in preweaned dairy cattle
Kern, J., Jorgensen, M. W., Boerman, J. P., Erasmus, M. A., Johnson, J. S., & Pempek, J. A. (2024) · Journal of Animal Science · doi:10.1093/jas/skae171 · Cited by 5 · see citing works
Wool cortisol concentrations trends in the lamb from birth to slaughter
Zoratti, A., Corazzin, M., Bodas, R., Domínguez, E., Geß, A., Prandi, A., & Peric, T. (2023) · Small Ruminant Research · doi:10.1016/j.smallrumres.2023.106988 · Cited by 4 · see citing works
Hair cortisol concentration of dairy cattle is unrelated to automation level of dairy farms—however, it can reflect Welfare Quality® measures
Lavrijsen-Kromwijk, L., Müller, U., Demba, S., Gimsa, U., & Rose, S. (2025) · Frontiers in Animal Science · doi:10.3389/fanim.2025.1688775 · Cited by 3 · see citing works
Post-milking application of a Lacticaseibacillus paracasei strain impacts bovine teat microbiota while preserving the mammary gland physiology and immunity
Goetz, C., Rault, L., Cuffel, J., Poton, P., Finot, L., Boullet, G., Boutinaud, M., & Even, S. (2024) · Beneficial Microbes · doi:10.1163/18762891-bja00014 · Cited by 3 · see citing works
Cardiac autonomic responses to transrectal examination and parlor milking of lame and nonlame dairy cows
Kovács, L. Á., Kézér, F. L., Ruff, F., Czirok, M., Bakony, M., & Jurkovich, V. (2024) · Journal of Dairy Science · doi:10.3168/jds.23674 · Cited by 3 · see citing works
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Leduc, A., Rau, A., Laloë, D., Guillou, S. L., Martin, P., Gelé, M., Pires, J., Faulconnier, Y., Leroux, C., Boutinaud, M., et al. (2025) · Molecular Omics · doi:10.1039/d4mo00190g · Cited by 2 · see citing works
Can we get information on dairy cow chronic stress biomarkers from milk mid-infrared spectra?
Grelet, C., Simon, H., Leblois, J., Christophe, O. S., Jattiot, M., Gaudillère, N., Reding, R., Wavreille, J., Strang, E. J. P., Auer, F.-J., et al. (2025) · Journal of Dairy Science · doi:10.3168/jds.2025-26502 · Cited by 2 · see citing works
Self-citation
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Wang, X. Q., Yuan, Y., Pei, F., Yang, J., Wang, C., Bao, P., Zhao, X., Liu, H., Gao, H., Hou, M., et al. (2025) · Animals · doi:10.3390/ani15203049 · Cited by 2 · see citing works
Determining Cortisol in Animal Hair as a Marker of Chronic Stress
Samsonova, J., Saushkin, N., & Piskunov, A. (2025) · Biology Bulletin Reviews · doi:10.1134/s207908642560078x · Cited by 2 · see citing works
Welfare and Health Challenges of ‘New Entry’ Dairying: a Practitioner’s Perspective
Chamberlain, P. (2023) · Animal welfare · doi:10.1007/978-3-031-21020-4_16 · Cited by 2 · see citing works
Effect of Milk-Feeding Frequency and Calcium Gluconate Supplementation on Growth, Health, and Reproductive and Metabolic Features of Holstein Heifers at a Rearing Farm
Revilla‐Ruiz, Á., Carulla, P., Fernández-Novo, A., de Mercado, E., Pérez‐Navarro, A., Patrón‐Collantes, R., Sebastián, F., Pérez‐Garnelo, S. S., González‐Martín, J. V., Estellés, F., et al. (2024) · Animals · doi:10.3390/ani14091336 · Cited by 4 · see citing works
Determination of heart rate variability as an indicator of the influence of autonomic nervous system tone in cows
Hryshchuk, I. А., Postoi, R., Horbay, R., Hryshchuk, A. V., & Karpovskyi, V. (2023) · Ukrainian journal of veterinary sciences · doi:10.31548/veterinary2.2023.43 · Cited by 1 · see citing works
Effect of Stress on Reproduction and Reproductive Technologies in Male and Female, Beef and Dairy Cattle
Pérez‐Garnelo, S. S., Utrilla, M. J., Fernández-Novo, A., Revilla‐Ruiz, Á., Villagrá, A., & Astiz, S. (2024) · Springer eBooks · doi:10.1007/978-3-031-73079-5_6 · Cited by 1 · see citing works
Replacing Soybean Meal with Hemp Leaves with Very Low THC Content in the Diet for Dairy Cows: Impact on Digestibility, Nitrogen Use Efficiency and Energy Metabolism
Schwerdtfeger, J., Görs, S., & Kuhla, B. (2025) · Animals · doi:10.3390/ani15111662 · Cited by 1 · see citing works
Fit-for-purpose validation of hair cortisol concentration as a biomarker of dairy cow welfare
Botia, M., Contreras-Aguilar, M. D., Cerón, J. M. C., Llonch, P., Berteselli, G. V., Canali, E., Frondelius, L., & Stygar, A. H. (2025) · Journal of Dairy Research · doi:10.1017/s0022029925101039 · Cited by 1 · see citing works
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Li, C., Chen, X., Fang, T., Gao, J., Zhao, G., & Gu, X. (2026) · Veterinary Sciences · doi:10.3390/vetsci13020134 · Cited by 1 · see citing works
Heat Stress in Dairy Cattle Production: A View from the Perspective of Sustainable Development
Mylostyvyi, R. (2026) · Sustainability · doi:10.3390/su18168210 · Cited by 1 · see citing works
Dead Newborn Calf Affects Behavior, Cortisol and Milk Production in Primiparous Dairy CowsPreprint
González-de-la-Vara, M. D. R., Anda, F. D., & Romano, M. C. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4195795
Dead newborn calf affects behavior, cortisol, milk production, and reproductive performance in primiparous dairy cows
González-de-la-Vara, M. D. R., Anda, F. D., & Romano, M. C. (2023) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2023.06.008
RETRACTED: Dynamics of hematological and oxidative parameters characterizing the nonspecific resistance of cows under technological stress
Deryugina, A. V., Ivashchenko, M. N., Danilova, D., Сергеевич, К. Р., Polozova, A. V., Золотова, М. В., & Таламанова, М. Н. (2024) · BIO Web of Conferences · doi:10.1051/bioconf/20248401029
Retracted
Determination of new welfare and stress indicators on cattle and pig farms based on previously published studies
Hristov, S., Cincović, M., Stanković, B. M., Djoković, R., Andric, O., & Nakov, D. (2024) · International Congress of the Mediterranean Federation for Health and Production of Ruminants (FeMeSPRum) · doi:10.5937/femesprumns24014h
Impact of a natural rubber-based scratcher as an environmental enrichment on the scratching behavior, cortisol level, and semen quality of stable male goats
Kimsakulvech, S., Sriphavatsarakom, P., Thaikoed, S., Oupala, W., Punkong, C., Prompiram, P., Saingkaew, S., Hayakijkosol, O., & Wongtawan, T. (2024) · Veterinary World · doi:10.14202/vetworld.2024.2443-2450
RETRACTED: Changes in blood biochemical parameters during the implementation of adaptation processes in pigs under technological stress
Garskaya, N., Tresnitskiy, S. N., Garanovich, I., & Tresnitskiy, A. (2024) · BIO Web of Conferences · doi:10.1051/bioconf/202413801015
Retracted
Changes in Leukocyte Indices of Holstein Cows Under Prolonged Heat Stress ConditionsPreprint
Mylostyvyi, R. (2025) · Qeios · doi:10.32388/9ogxdp.2
Changes in Leukocyte Indices of Holstein Cows Under Prolonged Heat Stress ConditionsPreprint
Mylostyvyi, R. (2025) · Qeios · doi:10.32388/9ogxdp.3
Effects of dietary supplementation with Nigella sativa L. on productivity and health in dairy cows
Enculescu, M., Sertu, S., & Nicolae, I. (2025) · Biotechnology in Animal Husbandry · doi:10.2298/bah2502131e
Serum α-Glucosidase Activity as a New Parameter of Negative Energy Balance in Dairy Cows
Bartling, B., Tröbner, T., Grone, L., & Schmicke, M. (2026) · Veterinary Sciences · doi:10.3390/vetsci13020122
Changes in leukocyte indices of Holstein cows under prolonged heat stress conditions
Mylostyvyi, R., Sejian, V., Іжболдіна, О. О., Sanzhara, R. A., Черненко, О. І., Dochkin, D. O., & Hoffmann, G. (2026) · Tropical Animal Health and Production · doi:10.1007/s11250-026-04910-4
Subclinical endometritis in dairy heifers experimentally infected with bovine gammaherpesvirus 4
Romeo, F., Sosa, E., Bartolomé, J. A., Bilbao, G., Cantón, G., Pereyra, S. B., Lobo, J. I., Yavorsky, M. S., Vispo, P. E., Burges, P. L., et al. (2026) · The Veterinary Journal · doi:10.1016/j.tvjl.2026.106604
Effect of the Use of Bovine Appeasing Substance on Immunological, Metabolic, and Oxidative Parameters of Postpartum Dairy Cows: Modulation of the Stress Axis
Fritzen, A., Deolindo, G. L., Nora, L., & da Silva, A. S. (2026) · Animals · doi:10.3390/ani16081185
Alterations in Blood Markers, Rumen Fermentation, and Microbiota Due to Heat Stress in Holstein Cows During the Dry Period and Early Lactation
Naing, Y. P., & Kim, S.-H. (2026) · Animals · doi:10.3390/ani16111682
Heat stress responses in dairy cows: a longitudinal study across multiple heat waves
Lemal, P., Grelet, C., Dehareng, F., Vanlierde, A., Decruyenaere, V., Soyeurt, H., Schroyen, M., & Gengler, N. (2026) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2026.104530
Self-citation
Noninvasive and minimally invasive approaches for acute and chronic stress assessment in dairy cattle.
Kovács, L., & Jurkovich, V. (2026) · Journal of Dairy Science · doi:10.3168/jds.2026-28898
Immunohematological parameters in cows depending on the functional state of the liver and the stage of the production cycle
Kuznetsova, E. O., Белоусов, А. И., Oparina, O. Y., Krasnoperov, A. S., & CHERNITSKIY, A. E. (2026) · Achievements of Science and Technology in Agro-Industrial Complex · doi:10.53859/02352451_2026_40_4_83
Effects of cow-calf contact during the first week and following separation on cows' behavior, feed-related parameters, and milk yield and composition
Kurek, J., Kurek, A., Harms, J., Zeiler, E., Bernhardt, H., & Steinhoff‐Wagner, J. (2026) · Journal of Dairy Science · doi:10.3168/jds.2026-28673
Investigating the Association Between Salivary Profiles, Production-Related Variables, and Daily Lying Time in Dairy Cows: A Pilot Study
Berteselli, G. V., Costa, E. D., Contreras-Aguilar, M. D., Filipe, J., López-Arjona, M., Rossi, G. P., Cerón, J. M. C., Tecles, F., & Canali, E. (2026) · Animals · doi:10.3390/ani16162621
Hair cortisol as a biomarker of chronic stress in periparturient dairy cattle: associations with health status, lactation, and metabolic profiles
Momy, N. J., Nipu, M. N. U., & Faruk, M. S. A. (2026) · Tropical Animal Health and Production · doi:10.1007/s11250-026-05371-5
Free-choice Mongolian herbal-mineral supplementation improves serum mineral, antioxidant, endocrine, and metabolic indices in rams with pica
Man, D., Chen, L., Ao, X., 张文广, & Na, R. (2026) · Frontiers in Veterinary Science · doi:10.3389/fvets.2026.1946016

Dairy cows stress assessment by using innovative biomarkers of herd management systems
Malašauskienė, D., Televičius, M., Urbutis, M., & Antanaitis, R. (2021) · Lithuanian University of Health Sciences
RESEARCH ARTICLE Heart Rate Variability as an Indicator of Chronic Stress Caused by Lameness in Dairy Cows
Kovács, L., Kézér, F. L., Jurkovich, V., Kulcsár-Huszenicza, M., & Tőzsér, J. (2016)
Chronic Stress in Cattle and Lameness as a Possible Chronic Stressor
Bua, K. (2013) · Hungarian Veterinary Archive
Can we get information on dairy cow chronic stress biomarkers from milk mid-infrared spectra?
Grelet, C., Simon, H., Leblois, J., Christophe, O. S., Jattiot, M., Gaudillère, N., Reding, R., Wavreille, J., Strang, E. J. P., Auer, F.-J., et al. (2025) · Journal of Dairy Science · doi:10.3168/jds.2025-26502 · Cited by 2 · see citing works
Self-citation
Some physiological and biochemical methods for acute and chronic stress evaluationin dairy cows
Trevisi, E., & Bertoni, G. (2009) · Italian Journal of Animal Science · doi:10.4081/ijas.2009.s1.265 · Cited by 85 · see citing works

Authors: Grelet, C., Vanden Dries, V., Leblois, J., Wavreille, J., Mirabito, L., Soyeurt, H., Franceschini, S., Gengler, N., Brostaux, Y., HappyMoo Consortium, & Dehareng, F.
Affiliations: Walloon Agricultural Research Centre (BE)
Association Wallonne des Eleveurs (BE)
Institut de l’Elevage (FR)
University of Liège (BE)
Corresponding author: Dehareng, F.
ORCID: Grelet, C.
Mirabito, L.
Soyeurt, H.
Franceschini, S.
Gengler, N.
Brostaux, Y.
Dehareng, F.
Venue: animal
Publisher: Elsevier BV
Published: 2022-05
Volume: 16
Issue: 5
Pages: 100502
ISSN: 1751-7311 (ISSN-L)
DOI: 10.1016/j.animal.2022.100502
OpenAlex: W4226189990
Cited by: 55
References: 72
Citations by year: 2026: 15 · 2025: 14 · 2024: 13 · 2023: 10 · 2022: 3
FWCI: 11.06
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: animal (publishedVersion, cc-by-nc-nd)
Research Square (acceptedVersion, cc-by)
PubMed (publishedVersion)
ORBi (University of Liège) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Interreg Europe (NWE730)
Walloon Region
Waalse Gewest
Topics: Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Effects of Environmental Stressors on Livestock
Health Sciences › Veterinary › Small Animals › Animal health and immunology
Keywords: chronic stress, dairy cattle, stress biomarkers, overstocking, feed competition, noise stress, milk yield, milk production loss, heart rate, salivary cortisol, hair cortisol, rumination, beta-endorphin, thyroxine, blood glucose, welfare analysis
MeSH terms: Animals, Cattle, Female, Hydrocortisone, Lactation, Milk, Biomarkers, Fructosamine

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Identification of chronic stress biomarkers in dairy cows

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