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Analysis of endogenous cortisol concentrations in the hair of rhesus macaques
Abstract
Short-term changes in activity of the hypothalamic-pituitary-adrenocortical (HPA) system are routinely assessed by measuring glucocorticoid or metabolite concentrations in plasma, saliva, urine, or feces. However, there are no current methods for determining long-term (i.e., weeks or months) activity of this system. Herein, we describe the development and validation of a simple procedure for measuring cortisol concentrations in the hair of rhesus macaques. This procedure involves two brief isopropanol washes of the hair strands to remove surface contaminants, subsequent powdering of the washed and dried hair, a 24-h methanol extraction followed by evaporation of the solvent and reconstitution of the extract in assay buffer, and finally analysis of the extracted cortisol by a sensitive and specific enzyme immunoassay. Our results confirm the specificity of the procedure for cortisol, show that proximal and distal segments of hair do not differ in their cortisol concentration, and demonstrate that a significant and prolonged stressful experience produces a significant increase in hair cortisol. This new procedure should be valuable for assessing baseline HPA activity in nonhuman primates (and, with appropriate validation, in other species as well) over relatively long periods of time, and also for monitoring chronic stress that might be associated with various experimental manipulations.
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“providing prospective validation of the hair cortisol method as a field-friendly biological marker of stress exposure”
From Chronic Stress, Hair Cortisol and Depression: A Prospective and Longitudinal Study of Medical Internship (2018) · cites this paper as Davenport et al., 2006
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Moody, S. N., van Dammen, L., Wang, W., Greder, K. A., Neiderhiser, J. M., Afulani, P. A., Willette, A. A., & Shirtcliff, E. A. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105805 · Cited by 36
A spontaneous depressive pattern in adult female rhesus macaques
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“Similarly, HCC in rhesus macaques correlated with saliva samples taken from animals that were trained for saliva collection (Davenport et al., 2006).”
Roelofs, S., Godding, L., de Haan, J. R., van der Staay, F. J., & Nordquist, R. E. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.12.014 · Cited by 38
“This kit has previously been validated for determining hair cortisol concentrations [12,36].”
Foyer, P., Svedberg, A.-M., Nilsson, E., Wilsson, E., Faresjö, Å., & Jensen, P. (2015) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2015.09.006 · Cited by 35
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
Nejad, J. G., Ghaffari, M. H., Ataallahi, M., Jo, J.-H., & Lee, H. (2022) · Animals · doi:10.3390/ani12223096 · Cited by 34
“[58], we developed an extraction method for measuring cortisol [8] and corticosterone [22] levels in our laboratory.”
MethodHair Cortisol, Perceived Stress and Dispositional Optimism: A Pilot Study among Adolescents
McConnell, R. (2014) · Journal of Traumatic Stress Disorders & Treatment · doi:10.4172/2324-8947.1000126 · Cited by 34
“Hair samples—At least 10mg (~50 strands of hair) was collected from the vertex posterior, where there is the most uniform growth pattern between individuals, using procedures previously developed [5].”
BackgroundMethodInfluentialCORTISOL 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
“In humans and horses, the cortisol level decreases along the hair shaft (21, 22) while no differences were found in rhesus macaques (12) or dogs (13).”
BackgroundMethodInfluentialEffects of demography and urbanization on stress and body condition in urban white-tailed deer
Potratz, E. J., Brown, J. S., Gallo, T., Anchor, C. L., & Santymire, R. M. (2019) · Urban Ecosystems · doi:10.1007/s11252-019-00856-8 · Cited by 34
“The majority of stress studies using hair do not test for age effects, as it can be difficult to acquire samples from all ages (Koren et al. 2002; Davenport et al. 2006; Accorsi et al. 2008; Ashley et al. 2011; Bryan et al. 2013).”
BackgroundBhopal, S., Verma, D., Roy, R., Soremekun, S., Kumar, D., Bristow, M., Bhanushali, A. A., Divan, G., & Kirkwood, B. R. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.05.012 · Cited by 35
Weaver, S., Hynd, P., Ralph, C. R., Edwards, J. E. H., Burnard, C. L., Narayan, E. J., & Tilbrook, A. J. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106503 · Cited by 34
Wïttchen, H., Schönfeld, S., Thurau, C., Trautmann, S., Galle, M., Mark, K., Hauffa, R., Zimmermann, P. L., Schaefer, J., Steudte‐Schmiedgen, S., et al. (2012) · International Journal of Methods in Psychiatric Research · doi:10.1002/mpr.1356 · Cited by 33
“Recently, hair cortisol has been validated as an index of long-term cortisol secretion in a number of human and animal studies (e.g. Davenport et al., 2006; Kirschbaum et al., 2009; Stalder et al., 2010; Thomson et al., 2010).”
BackgroundNarayan, E. J., Parnell, T., Clark, G., Martin-Vegue, P., Mucci, A., & Hero, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.002 · Cited by 35
“, 2003), hair (Davenport et al., 2006) or faecal samples (Narayan et al.”
Kapoor, A., Lubach, G. R., Hedman, C. J., Ziegler, T. E., & Coe, C. L. (2014) · Pediatric Research · doi:10.1038/pr.2014.1 · Cited by 33
The effect of ACTH upon faecal glucocorticoid excretion in the koala
Davies, N., Gillett, A. K., McAlpine, C., Seabrook, L., BAXTER, G. S., Lunney, D., & Bradley, A. J. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0123 · Cited by 32
“Therefore, specific point measurements may be unrepresentative of long-term hormone exposure levels (Harper & Austad 2000, Davenport et al. 2006).”
Drury, S. S., Howell, B., Jones, C., Esteves, K. C., Morin, E. L., Schlesinger, R. P., Meyer, J. S., Baker, K. C., & Sánchez, M. M. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001225 · Cited by 33
Fürtbauer, I., Solman, C., & Fry, A. (2019) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2018.12.009 · Cited by 27
Hair Cortisol in Sheltered Cows and Its Association with Other Welfare Indicators
Sharma, A., Umapathy, G., Kumar, V., & Phillips, C. J. C. (2019) · Animals · doi:10.3390/ani9050248 · Cited by 33
“[10] and modified by Tallo-Parra et al.”
BackgroundMeasuring hair and blood cortisol in sheep and dairy cattle using RIA and ELISA assay: a comparison
Nejad, J. G., Park, K.-H., Forghani, F., Lee, H., Lee, J., & Sung, K. (2019) · Biological Rhythm Research · doi:10.1080/09291016.2019.1611335 · Cited by 33
“A similar equation has been suggested by Davenport et al. (2006) and Ghassemi Nejad et al. (2019) in order to convert results from μg/dL to pg/mg as follows: ug=dLð Þ=100ð Þ 0:025ð Þ 1000=600ð Þ 400=25ð Þ= powder weight 1000ð Þð Þ 1000 As for the RIA, the procedure was as follows: 1.”
Nonhuman primate abnormal behavior: Etiology, assessment, and treatment
Lutz, C. K., Coleman, K., Hopper, L. M., Novak, M. A., Perlman, J. E., & Pomerantz, O. (2022) · American Journal of Primatology · doi:10.1002/ajp.23380 · Cited by 39
“Behavioral monitoring can be supplemented with other measures such as fecal hormones or hair cortisol (M. D. Davenport et al., 2006; Rimbach et al., 2013); as well as tests of mood and affect (Cassidy et al., 2021; Pomerantz et al., 2012); however, these methodologies are outside of the scope of…”
MethodGleeson, J., Lederman, R., Herrman, H., Koval, P., Eleftheriadis, D., Bendall, S., Cotton, S. M., & Alvarez-Jimenez, M. (2017) · Trials · doi:10.1186/s13063-016-1775-5 · Cited by 33
“Mean baseline HPA system activity during the last month is measured by a validated procedure for measuring hair cortisol [48].”
BackgroundMethodFeasibility of Hair Collection for Cortisol Measurement in Population Research on Adolescent Health
Ford, J. L., Boch, S. J., & McCarthy, D. O. (2016) · Nursing Research · doi:10.1097/nnr.0000000000000154 · Cited by 32
Fuchs, A., Jaite, C., Neukel, C., Dittrich, K., Bertsch, K., Kluczniok, D., Möhler, E., Attar, C. H., Brunner, R. M., Bödeker, K., et al. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.02.003 · Cited by 31
Jewgenow, K., Azevedo, A., Albrecht, M., Kirschbaum, C., & Dehnhard, M. (2020) · Conservation Physiology · doi:10.1093/conphys/coaa009 · Cited by 30
“Our data on hair analysis in wildlife species contribute to the growing data base of studies that aim to use hGC (Koren et al., 2002; Davenport et al., 2006; Accorsi et al., 2008; Comin et al., 2011) to evaluate chronic stress, in most of which assays based on antibodies directed against cortisol have been applied (Ko…”
BackgroundEerdenburg, F. J. C. M. V., Hof, T., Doeve, B. H., Ravesloot, L., Zeinstra, E. C., Nordquist, R. E., & van der Staay, F. J. (2021) · Animals · doi:10.3390/ani11030821 · Cited by 32
“Some studies report increased HPA axis response during chronic stress [26,44], while others describe a blunted HPA axis response [26,29].”
BackgroundPsychological and Physiological Responses following Repeated Peer Death
Andersen, J. P., Silver, R. C., Stewart, B. T., Koperwas, B., & Kirschbaum, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075881 · Cited by 37
“The Davenport protocol was employed for washing hair and steroid extraction [19].”
Performance of ad libitum fed dairy calves weaned using fixed and individual methods
Welboren, A. C., Leal, L. N., Steele, M. A., Khan, M. A., & Martín‐Tereso, J. (2019) · animal · doi:10.1017/s1751731119000181 · Cited by 32
Fourie, N. H., Jolly, C. J., Phillips‐Conroy, J. E., Brown, J. L., & Bernstein, R. M. (2015) · Primates · doi:10.1007/s10329-015-0469-z · Cited by 31
Veronesi, M. C., Comin, A., Meloni, T., Faustini, M., Rota, A., & Prandi, A. (2015) · Theriogenology · doi:10.1016/j.theriogenology.2015.05.013 · Cited by 31
Pearson, B. L., Judge, P. G., & Reeder, D. M. (2008) · American Journal of Primatology · doi:10.1002/ajp.20613 · Cited by 34
“An alternative to plasma sampling is noninvasive assessment of cortisol levels in feces, urine, and hair [Davenport et al., 2006; Queyras & Carosi, 2004].”
BackgroundDisturbance and chronic levels of cortisol in boreal woodland caribou
Ewacha, M. V. A., Roth, J. D., Anderson, W. G., Brannen, D., & Dupont, D. L. J. (2017) · Journal of Wildlife Management · doi:10.1002/jwmg.21288 · Cited by 31
Social rank and cortisol among female rhesus macaques ( Macaca mulatta )
Qin, D., Joshua, D. R., XiaoLi, F., Xun-Xun, C., Shang-chuan, Y., Chun-Lu, L., Lv, L., Yuan-ye, M., & Xin-Tian, H. (2013) · Zoological Research · doi:10.3724/sp.j.1141.2013.e02e42 · Cited by 30
“This makes cortisol measured in hair a biomarker of chronic stress, as demonstrated previously in two studies of rhesus macaques in which hair samples were obtained to assess long-term stress levels (Davenport et al, 2006; Feng et al, 2011).”
BackgroundMethodInfluentialMeasurement of cortisol in dog hair: a noninvasive tool for the diagnosis of hypercortisolism
Ouschan, C., Kuchar, A., & Möstl, E. (2013) · Veterinary Dermatology · doi:10.1111/vde.12043 · Cited by 30
Hamel, A. F., Lutz, C. K., Coleman, K., Worlein, J. M., Peterson, E. J., Rosenberg, K. L., Novak, M. A., & Meyer, J. S. (2016) · American Journal of Primatology · doi:10.1002/ajp.22526 · Cited by 30
“Fortunately, this limitation has been overcome by the development and validation of hair cortisol measurement by our laboratory and others [Davenport et al., 2006; Kirschbaum et al., 2009; Raul et al., 2004; Sauv e et al., 2007].”
MethodMorgan, L., Itin‐Shwartz, B., Koren, L., Meyer, J. S., Matas, D., Younis, A., Novak, S., Weizmann, N., Rapaic, O., Ahmad, W. A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-52677-6 · Cited by 30
Effects of environmental enrichment on decision-making behavior in pigs
van der Staay, F. J., van Zutphen, J. A., de Ridder, M. M., & Nordquist, R. E. (2017) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2017.05.006 · Cited by 31
“Then, each pig was picked up and held by one experimenter, and the other shaved the fl ank of the pig to collect between 0.5 and 1 g of hair as described by Davenport et al. (2006).”
InfluentialWelfare in a shelter dog rehomed with Alzheimer patients
Piva, E., Liverani, V., Accorsi, P. A., Sarli, G., & Gandini, G. (2008) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2007.08.004 · Cited by 30
Woolsey, I. D., Jensen, P., Deplazes, P., & Kapel, C. M. O. (2015) · Parasitology International · doi:10.1016/j.parint.2015.08.006 · Cited by 29
Rolland, R. M., Graham, K. M., Stimmelmayr, R., SUYDAM, R. S., & George, J. C. (2019) · Marine Mammal Science · doi:10.1111/mms.12596 · Cited by 29
Lagoda, M. E., Marchewka, J., O’Driscoll, K., & Boyle, L. A. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.883154 · Cited by 32
“Doing so allows patterns to be identified, which in turn can reveal deviations from the norm, indicative of chronic stress (31, 32, 34).”
BackgroundMethodInfluentialZhang, G., Li, L., Kong, Y., Xu, D., Bao, Y., Zhang, Z., Liao, Z., Jiao, J., Fan, D., Long, X., et al. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2023.02.049 · Cited by 30
“The sample preparation procedures are described in previous studies.(40,44) The CSF was obtained through a needle inserted between the 3rd and 4th lumbar vertebrae.”
MethodHair cortisol predicts object permanence performance in infant rhesus macaques (Macaca mulatta)
Dettmer, A. M., Novak, M. F. S. X., Novak, M. A., Meyer, J. S., & Suomi, S. J. (2009) · Developmental Psychobiology · doi:10.1002/dev.20405 · Cited by 30
“…Lutz, Novak, & Meyer, 2006), which reflects cortisol concentrations over several months and, more importantly, can be used to study responses to major life stressors in these subjects (e.g., housing relocation; Davenport et al., 2006; Davenport, Lutz, Tiefenbacher, Novak, & Meyer, 2008).”
MethodInfluentialNoppe, G., van Rossum, E. F. C., Vliegenthart, J., Koper, J. W., & van den Akker, E. L. T. (2014) · Clinical Endocrinology · doi:10.1111/cen.12551 · Cited by 33
Bechshoft, T., Wright, A., Weisser, J., Teilmann, J., Dietz, R., Hansen, M., Björklund, E., & Styrishave, B. (2015) · Conservation Physiology · doi:10.1093/conphys/cov016 · Cited by 29
“However, substantial differences in inter-individual cortisol concentrations are commonly observed in other matrices, such as blood and hair (Tryland et al., 2002; Haave et al., 2003; Davenport et al., 2006; Suavé et al., 2007; Eskesen et al., 2009).”
Behavioral and physiological response to onset and termination of social instability in female mice
Jarcho, M. R., Massner, K., Eggert, A., & Wichelt, E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.004 · Cited by 29
“cortisol in primates, corticosterone in rodents) in hair, however, is a relatively new technique that allows for the non-invasive assessment of biomarkers representing a longer period of HPA activity, and has been shown to accurately reflect individual responses to various social stressors in rhesus macaques (Davenpor…”
BackgroundMethodInfluentialIncreased blubber cortisol in ice-entrapped beluga whales (Delphinapterus leucas)
Trana, M. R., Roth, J. D., Tomy, G. T., Anderson, W. G., & Ferguson, S. H. (2015) · Polar Biology · doi:10.1007/s00300-015-1881-y · Cited by 29
“By measuring stress hormones in tissues that reflect long-term exposure to stressors, it is possible to monitor changes in the stress experienced by individuals over prolonged time periods (Davenport et al. 2006; Bortolotti et al. 2008; Saco et al. 2008; Okuliarová et al. 2010).”
BackgroundVentrella, D., Elmi, A., Barone, F., Carnevali, G., Govoni, N., & Bacci, M. L. (2018) · Animals · doi:10.3390/ani8070113 · Cited by 31
“One of the biggest limitations to hematic CORT quantification lies in the ultra-fast activation of the hypothalamic-pituitary-adrenocortical (HPA) system during stressful events [10], making it almost useless when assessing environmental chronic stressors.”
BackgroundMartins‐Silva, T., Martins, R. C., Murray, J., Carvalho, A. M., Rickes, L. N., Corrêa, B. D. F., Fraga, B. B., Brum, C. B., Freitas, D. F., Meyer, F. D. T., et al. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107185 · Cited by 31
Wooddell, L. J., Kaburu, S., Rosenberg, K. L., Meyer, J. S., Suomi, S. J., & Dettmer, A. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157108 · Cited by 28
“Hair samples were collected by shaving the back of the animals’ necks [36] during routine health exams in August 2014 and February 2015 for all 49 subjects across the three matrilines.”
MethodAssay validation of hair androgens across the menstrual cycle
Wang, W., Moody, S. N., Kiesner, J., Appiani, A. T., Robertson, O. C., & Shirtcliff, E. A. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.10.029 · Cited by 28
Emotion regulation moderates the association between parent and child hair cortisol concentrations
Kao, K., Tuladhar, C. T., Meyer, J. S., & Tarullo, A. R. (2019) · Developmental Psychobiology · doi:10.1002/dev.21850 · Cited by 28
Boyle, S., de la Sancha, N. U., Pérez, & Kabelik, D. (2021) · Scientific Reports · doi:10.1038/s41598-021-81073-2 · Cited by 21
Lines, R. L. J., Ducker, K. J., Ntoumanis, N., Thøgersen‐Ntoumani, C., Fletcher, D., & Gucciardi, D. F. (2021) · Psychophysiology · doi:10.1111/psyp.13846 · Cited by 35
Novak, M. A., Hamel, A. F., Coleman, K., Lutz, C. K., Worlein, J. M., Menard, M. T., Ryan, A., Rosenberg, K. L., & Meyer, J. S. (2014) · PubMed Central · Cited by 28
Fardi, S., Sauther, M. L., Cuozzo, F. P., Jacky, I. A. Y., & Bernstein, R. M. (2017) · American Journal of Primatology · doi:10.1002/ajp.22731 · Cited by 30
“There are currently two primary ways of processing hair: manually (Fourie & Bernstein, 2011) and with a ball mill (Davenport et al., 2006) that affect measurement of absolute concentrations of cortisol, even if the final patterns and correlations are similar.”
BackgroundMethodInfluentialNejad, J. G., Ataallahi, M., & Park, K.-H. (2019) · Journal of Animal Science and Technology · doi:10.5187/jast.2019.61.1.41 · Cited by 28
“The application of SS in finely cutting hair was reported in several studies [5, 14, 15].”
BackgroundResultLeppänen, M. H., Sääksjärvi, K., Vepsäläinen, H., Ray, C., Hiltunen, P., Koivusilta, L., Erkkola, M., Sajaniemi, N., & Roos, E. (2020) · European Journal of Pediatrics · doi:10.1007/s00431-020-03686-5 · Cited by 26
“[26] for the washing of hair and steroid extraction.”
BackgroundWoolsey, I. D., Bune, N. E. T., Jensen, P., Deplazes, P., & Kapel, C. M. O. (2015) · Parasitology Research · doi:10.1007/s00436-015-4355-9 · Cited by 27
“…has been used as a biological marker in a number of animals including rhesus macaques, dogs and cats with these studies concluding that salivary (Davenport et al. 2006), faecal (Accorsi et al. 2008) and hair cortisol measurements reflect (at least to a certain extent) the same adrenal activity.”
BackgroundMethodInfluentialTennenhouse, E. M., Putman, S. B., Boisseau, N. P., & Brown, J. L. (2016) · Primates · doi:10.1007/s10329-016-0566-7 · Cited by 28
“Hair has been widely used to quantify steroid hormones in haplorhine primates (Davenport et al. 2006; Dettmer et al. 2012, 2014; Kapoor et al. 2014; Fourie and Bernstein 2011; Carlitz et al. 2014).”
BackgroundMethodInfluentialWang, X., Busch, J. R., Banner, J., Línnet, K., & Johansen, S. S. (2019) · Forensic Science International · doi:10.1016/j.forsciint.2019.109968 · Cited by 29
Hair cortisol in horses (Equus caballus) in relation to management regimes, personality, and breed
Sauveroche, M., Henriksson, J., Theodorsson, E., Holm, A.-C. S., & Roth, L. S. V. (2020) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2019.12.002 · Cited by 27
Applying minimally invasive biomarkers of chronic stress across complex ecological contexts
DeCaro, J. A., & Helfrecht, C. (2022) · American Journal of Human Biology · doi:10.1002/ajhb.23814 · Cited by 28
“Although hair hormone analysis has a long history, Davenport et al. (2006) were among the first to validate its use in rhesus macaques for studies of cortisol and their methodology has been adapted for use in humans.”
BackgroundMethodInfluentialSharpley, C. F., Kauter, K., & McFarlane, J. R. (2010) · Physiological Research · doi:10.33549/physiolres.931874 · Cited by 28
Vandeleest, J. J., Capitanio, J. P., Hamel, A. F., Meyer, J. S., Novak, M. A., Mendoza, S. P., & McCowan, B. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.10.008 · Cited by 27
“…et al., 2012), mammalian wildlife (Ashley et al., 2011; Bechshøft et al., 2011; Koren et al., 2008; Martin and Réale, 2008), non- human primates (Davenport et al., 2006; Dettmer et al., 2014; Hamel et al., 2011; Laudenslager et al., 2011), and humans (e.g. D’Anna-Hernandez et al., 2011;…”
BackgroundMethodInfluentialHair or salivary cortisol analysis to identify chronic stress in piglets?
Prims, S., Hole, C. V., Cruchten, S. J. M. V., Ginneken, C. J. V., Ostade, X. V., & Casteleyn, C. R. (2019) · The Veterinary Journal · doi:10.1016/j.tvjl.2019.105357 · Cited by 26
Fusi, J., Peric, T., Probo, M., Cotticelli, A., Faustini, M., & Veronesi, M. C. (2021) · Animals · doi:10.3390/ani11061632 · Cited by 26
Assessing stress in Western Hudson Bay polar bears using hair cortisol concentration as a biomarker
Mislan, P., Derocher, A. E., Louis, V. L. S., Richardson, E. S., Lunn, N. J., & Janz, D. M. (2016) · Ecological Indicators · doi:10.1016/j.ecolind.2016.06.034 · Cited by 28
A longitudinal study of hair cortisol concentrations inMacaca nemestrinamothers and infants
Grant, K. S., Worlein, J. M., Meyer, J. S., Novak, M. A., Kroeker, R., Rosenberg, K. L., Kenney, C., & Burbacher, T. M. (2016) · American Journal of Primatology · doi:10.1002/ajp.22591 · Cited by 29
Stressed-Out Oral Immunity: A Gateway From Socioeconomic Adversity to Periodontal Disease
Gomaa, N., Glogauer, M., Nicolau, B., Tenenbaum, H., Siddiqi, A., Fine, N., & Quiñonez, C. (2020) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000774 · Cited by 25
Jones, J. K., Turner, M. J., & Barker, J. B. (2020) · International Journal of Stress Management · doi:10.1037/str0000218 · Cited by 29
Hair Cortisol as a Biomarker of Stress in the 2011 Libyan War
Etwel, F., Russell, E., Rieder, M. J., Uum, S. H. V., & Koren, G. (2014) · Clinical and investigative medicine · doi:10.25011/cim.v37i6.22245 · Cited by 25
“Adding strong evidence that cortisol does not naturally vary in distribution along the length of the hair shaft, studies using both rhesus macaques [27] and dogs [28] found no significant differences between the most proximal half and the most distal half of the hair shaft.”
BackgroundRelocation and Hair Cortisol Concentrations in New Zealand White Rabbits
Peric, T., Comin, A., Corazzin, M., Montillo, M., Canavese, F., Stebel, M., & Prandi, A. (2016) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2016.1183489 · Cited by 25
“Moreover, even in the other species (Davenport et al., 2006, 2008; Fairbanks et al., 2011) in which the premove and postmove hair cortisol concentrations were studied, low variations between animals were observed.”
BackgroundQiviut cortisol in muskoxen as a potential tool for informing conservation strategies
Francesco, J. D., Navarro-González, N., Wynne‐Edwards, K. E., Peacock, S. J., Leclerc, L., Tomaselli, M., Davison, T., Carlsson, A. M., & Kutz, S. J. (2017) · Conservation Physiology · doi:10.1093/conphys/cox052 · Cited by 27
“Similarly, among free-ranging elk (Cervus canadensis) in South Dakota, USA, FGM concentrations were at their lowest in winter and peaked in the summer, conceivably due to increased human disturbance, high temperatures, or normal seasonal metabolic patterns (Millspaugh et al., 2001).”
MethodInfluentialProgesterone and Cortisol Levels in Blood and Hair of Wild Pregnant Red Deer (Cervus Elaphus) Hinds
Ventrella, D., Elmi, A., Bertocchi, M., Aniballi, C., Parmeggiani, A., Govoni, N., & Bacci, M. L. (2020) · Animals · doi:10.3390/ani10010143 · Cited by 24
“Blood cortisol levels change quickly throughout the day and are therefore relatively unreliable, but quantification in matrices such as feces and hair seems to be a good indicator of chronic stress, potentially also related to the reproductive status of the animal [16,23].”
Backgroundvan Ockenburg, S. L., Schenk, H., van der Veen, A., van Rossum, E. F. C., Kema, I. P., & Rosmalen, J. G. M. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.07.220 · Cited by 24
Kroshko, T., Kapronczai, L., Cattet, M., Macbeth, B. J., Stenhouse, G. B., Obbard, M. E., & Janz, D. M. (2017) · MethodsX · doi:10.1016/j.mex.2017.01.004 · Cited by 24
“As described previously [7,8], a single wash cycle consisted of the hair being mixed with 2.”
BackgroundResultInfluentialInvestigating Relationships between Reproduction, Immune Defenses, and Cortisol in Dall Sheep
Downs, C. J., Boan, B. V., Lohuis, T., & Stewart, K. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00105 · Cited by 25
“Briefly, hair glucocorticoid concentrations are sensitive to major prolonged stressors and are correlated with changes in circulating glucocorticoids observed during pregnancy (43, 46, 47).”
BackgroundMethodEffect of Overcrowding on Hair Corticosterone Concentrations in Juvenile Male Wistar Rats.
Uarquin, D. G., Meyer, J. S., Cárdenas, F. P., & Rojas, M. J. (2016) · PubMed Central · Cited by 24
Hair cortisol levels determined at different body sites in the New Zealand White rabbit
Comin, A., Zufferli, V., Peric, T., Canavese, F., Barbetta, D., & Prandi, A. (2012) · World Rabbit Science · doi:10.4995/wrs.2012.1106 · Cited by 24
Cortisol levels in cats’ hair in presence or absence of Microsporum canis infection
Galuppi, R., Leveque, J. F. C., Beghelli, V., Bonoli, C., Mattioli, M., Ostanello, F., Tampieri, M. P., & Accorsi, P. A. (2013) · Research in Veterinary Science · doi:10.1016/j.rvsc.2013.07.023 · Cited by 24
Relocation stress induces short-term fecal cortisol increase in Tonkean macaques (Macaca tonkeana)
Cinque, C., Marco, A. D., Mairesse, J., Giuli, C., Sanna, A., Marco, L. D., Zuena, A. R., Casolini, P., Catalani, A., Thierry, B., et al. (2016) · Primates · doi:10.1007/s10329-016-0590-7 · Cited by 23
Fischer‐Tenhagen, C., Wiegard, M., Heuwieser, W., & Thöne‐Reineke, C. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-13967 · Cited by 23
King, L. S., Humphreys, K. L., Cole, D. A., & Gotlib, I. H. (2021) · Comprehensive Psychoneuroendocrinology · doi:10.1016/j.cpnec.2021.100102 · Cited by 23
“For washing of hair and steroid extraction, the protocol of Daven-port, Tiefenbacher, Lutz, Novak, and Meyer [28] was used; HCC in each 1-cm segment was estimated using a commercially available immuno-assay with chemiluminescence detection (CLIA, IBL-Hamburg, Germany; intra-and inter-assay…”
MethodVas, J., Chojnacki, R. M., Kjøren, M. F., Lyngwa, C., & Andersen, I. L. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.04.009 · Cited by 23
Novak, M. A., Menard, M. T., El‐Mallah, S. N., Rosenberg, K. L., Lutz, C. K., Worlein, J. M., Coleman, K., & Meyer, J. S. (2016) · American Journal of Primatology · doi:10.1002/ajp.22547 · Cited by 23
“more recent approach involves measuring cortisol in hair [Davenport et al., 2006].”
BackgroundMethodFactors influencing alopecia and hair cortisol in rhesus macaques (Macaca mulatta)
Lutz, C. K., Coleman, K., Worlein, J. M., Kroeker, R., Menard, M. T., Rosenberg, K. L., Meyer, J. S., & Novak, M. A. (2016) · Journal of Medical Primatology · doi:10.1111/jmp.12220 · Cited by 23
Simmons, J. G., Schwartz, O., Bray, K. O., Deane, C., Pozzi, E., Richmond, S., Smith, J., Vijayakumar, N., Byrne, M. L., Seal, M. L., et al. (2017) · BMC Pediatrics · doi:10.1186/s12887-017-0905-x · Cited by 23
“Hair assays for the baseline assessment were conducted by Stratech Scientific and processed and assayed as described previously [76], using Salimetrics ELISA kits for cortisol, DHEA and testosterone.”
MethodFrugé, A. D., Cases, M. G., Howell, C. R., Tsuruta, Y., Smith-Johnston, K., Moellering, D. R., & Demark‐Wahnefried, W. (2017) · Cancer Causes & Control · doi:10.1007/s10552-017-0989-5 · Cited by 23
“1 3 of hair) [20], and has shown mixed correlations to urine [21] and salivary samples [22].”
BackgroundLife expectancy, family constellation and stress in giant mole-rats ( Fukomys mechowii )
Begall, S., Nappe, R., Hohrenk-Danzouma, L. L., Schmidt, T. C., Burda, H., Sahm, A., Szafranski, K., Dammann, P., & Henning, Y. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0207 · Cited by 23
“Therefore, we developed a decontamination protocol based on previously published protocols specifically validated for hair cortisol extraction [39,40]:”
MethodVerheyen, V., Remy, S., Govarts, E., Colles, A., Martin, L. R., Koppen, G., Voorspoels, S., Bruckers, L., Bijnens, E., Vos, S., et al. (2021) · Toxics · doi:10.3390/toxics9100245 · Cited by 23
“Strong positive associations between HCC and mean salivary cortisol levels, obtained through repeated sampling, were first established in animals and confirmed in humans [32,33].”
BackgroundGeß, A., Viola, I., Miretti, S., Macchi, E., Perona, G. E., Battaglini, L. M., & Baratta, M. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.00651 · Cited by 22
Shi, R., Dou, J., Liu, J., Sammad, A., Luo, H., Wang, Y., Guo, G., & Wang, Y. (2021) · Journal of Dairy Science · doi:10.3168/jds.2019-17856 · Cited by 22
Should stress management be part of the clinical care provided to chronically ill dogs?
Nicholson, S., & Meredith, J. E. (2015) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2015.09.002 · Cited by 22
“Hair samples were not washed before the extraction 175 process as washing may remove cortisol from the interior of the hair shaft 176 (Davenport et al., 2006, Gow et al., 2010).”
BackgroundMethodInfluentialAn Investigation of Hair Cortisol Concentration across Body Sites and within Hair shaft
Sharpley, C. F., Kauter, K., & McFarlane, J. R. (2010) · Clinical Medicine Insights Endocrinology and Diabetes · doi:10.4137/cmed.s4465 · Cited by 22
“There was a significant difference between subjects’ hair cortisol concentrations (F(9, 35) = 2.”
Yang, J., Li, J., Xu, G., Zhang, J., Chen, Z., Lu, Z., & Deng, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150729 · Cited by 22
Lockwood, S. A., Kattesh, H. G., Rhinehart, J., Strickland, L. G., Krawczel, P. D., Wilkerson, J. B., Kirkpatrick, F. D., & Saxton, A. M. (2016) · Theriogenology · doi:10.1016/j.theriogenology.2016.10.019 · Cited by 23
Schrock, A. E., Leard, C. N., Lutz, M. C., Meyer, J. S., & Gazes, R. P. (2019) · American Journal of Primatology · doi:10.1002/ajp.23001 · Cited by 24
Improving canine welfare in commercial breeding (CB) operations: Evaluating rehoming candidates
Stella, J. L., Shreyer, T., Ha, J. C., & Croney, C. (2019) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2019.104861 · Cited by 25
Metadata
- Authors
- Davenport, M. D., Tiefenbacher, S., Lutz, C. K., Novak, M. A., & Meyer, J. S.
- Affiliations
- Harvard University (US)
- University of Massachusetts Amherst (US)
- Corresponding author
- Meyer, Jerrold S.
- Venue
- General and Comparative Endocrinology
- Publisher
- Elsevier BV
- Published
- 2006-07
- Volume
- 147
- Issue
- 3
- Pages
- 255-261
- ISSN
- 0016-6480 (ISSN-L)
- OpenAlex
- W2074364102
- Cited by
- 659
- References
- 31
- Citations by year
- 2026: 18 · 2025: 29 · 2024: 33 · 2023: 41 · 2022: 35 · 2021: 53 · 2020: 44 · 2019: 73 · 2018: 33 · 2017: 52 · 2016: 53 · 2015: 35 · 2014: 31 · 2013: 28 · 2012: 30
- FWCI
- 3.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- General and Comparative Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (#RR11122, RR00 168, R24RR011122)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Behavior and Welfare Studies
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Keywords
- hair cortisol, rhesus monkeys, hypothalamic-pituitary-adrenal axis, chronic stress, non-human primates, stress biomarkers, enzyme immunoassay validation
- MeSH terms
- Animals, Hair, Hydrocortisone, Immunoenzyme Techniques, Macaca mulatta, Male, Saliva, Sensitivity and Specificity, Skin, Stress, Physiological, Time Factors
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