Cited by 659Stress Responses and CortisolAnimal Behavior and Welfare StudiesAdrenal Hormones and Disorders

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Analysis of endogenous cortisol concentrations in the hair of rhesus macaques

Davenport, Matthew D., Tiefenbacher, Stefan, Lutz, Corrine K., Novak, Melinda A., Meyer, Jerrold S.·2006·General and Comparative Endocrinology

DOI 10.1016/j.ygcen.2006.01.005

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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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What’s in a whisker? High-throughput analysis of twenty-eight C19 and C21 steroids in mammalian whiskers by ultra-performance convergence chromatography-tandem mass spectrometry
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A pilot trial of moderated online social therapy for family and friends of young people with borderline personality disorder features
Gleeson, J., Álvarez‐Jiménez, M., Betts, J. K., McCutcheon, L., Jovev, M., Lederman, R., Herrman, H., Cotton, S., Bendall, S., McKechnie, B., et al. (2020) · Early Intervention in Psychiatry · doi:10.1111/eip.13094 · Cited by 17
“Hair cortisol concentration was used as a biomarker of stress in carers (van Uum et al., 2008) via long-term alterations in basal hypothalamic–pituitary– adrenal (HPA) axis activity (Davenport et al., 2006).”
MethodInfluential
Effects of social tolerance on stress: hair cortisol concentrations in the tolerant Tonkean macaques (Macaca tonkeana) and the despotic long-tailed macaques (Macaca fascicularis)
Sadoughi, B., Lacroix, L., Berbesque, J. C., Meunier, H., & Lehmann, J. (2021) · Stress · doi:10.1080/10253890.2021.1998443 · Cited by 19
“Currently, studies on long-term cortisol (the main GC hormone in primate) concentrations are heavily skewed toward species with strict hierarchies (Davenport et al., 2006; Dettmer et al., 2014; Feng et al., 2016; Linden et al., 2019; Wooddell et al., 2016) and little is known about the distribution…”
BackgroundResult
Analysis of hair steroid hormones in polar bears (Ursus maritimus) via liquid chromatography–tandem mass spectrometry: comparison with two immunoassays and application for longitudinal monitoring in zoos
Hein, A. C., Baumgartner, K., von Fersen, L., Bechshøft, T., Woelfing, B., Kirschbaum, C., Mastromonaco, G. F., Greenwood, A. D., & Siebert, U. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113837 · Cited by 15
Hair cortisol and testosterone concentrations and semen production of Bos taurus bulls
Stradaioli, G., Peric, T., Montillo, M., Comin, A., Corazzin, M., Veronesi, M. C., & Prandi, A. (2017) · Italian Journal of Animal Science · doi:10.1080/1828051x.2017.1303339 · Cited by 15
“Those results documented that not only stress is associated with increased HCC, but also that hair cortisol content responds dynamically to changes in cortisol over time (Davenport et al. 2006, 2008).”
Background
Atypical experiences of captive chimpanzees (Pan troglodytes) are associated with higher hair cortisol concentrations as adults
Jacobson, S. L., Freeman, H. D., Santymire, R. M., & Ross, S. R. (2017) · Royal Society Open Science · doi:10.1098/rsos.170932 · Cited by 15
Sex differences in the impact of social status on hair cortisol concentrations in rhesus monkeys (Macaca mulatta)
Vandeleest, J. J., Winkler, S. L., Beisner, B. A., Hannibal, D. L., Atwill, E. R., & McCowan, B. (2019) · American Journal of Primatology · doi:10.1002/ajp.23086 · Cited by 15
Behavioral Disorders of Nonhuman Primates
Novak, M. A., Kelly, B. J., Bayne, K. A. L., & Meyer, J. S. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-381365-7.00007-8 · Cited by 15
Stress in the city? Coyote hair cortisol varies with intrinsic and extrinsic factors within a heavily urbanized landscape
Robertson, K. E., Ellington, E. H., Tonra, C. M., & Gehrt, S. D. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.165965 · Cited by 14
Exposure to the Indian Ocean Tsunami shapes the HPA-axis resulting in HPA “burnout” 14 years later
Lawton, R. I., Frankenberg, E., Seeman, T. E., Crimmins, E. M., Sumantri, C. S., & Thomas, D. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2306497120 · Cited by 16
“Hair samples were ground in a laboratory in Yogyakarta, Indonesia, following methods derived from Davenport et al. (50).”
Non-invasive methods for analysing pig welfare biomarkers
Svoboda, M., Němečková, M., Medkova, D., Sardi, L., & Hodkovicova, N. (2024) · Veterinární Medicína · doi:10.17221/17/2024-vetmed · Cited by 10
“Most of the published studies used isopropanol for hair washing, following the method described by Davenport et al. (2006).”
BackgroundMethod
Compatibility of preparatory procedures for the analysis of cortisol concentrations and stable isotope (δ13C, δ15N) ratios: a test on brown bear hair
Sergiel, A., Hobson, K. A., Janz, D. M., Cattet, M., Selva, N., Kapronczai, L., Gryba, C., & Zedrosser, A. (2017) · Conservation Physiology · doi:10.1093/conphys/cox021 · Cited by 14
“Hair or feather GC concentrations are increasingly applied to evaluate chronic exposure to various stressors or potentially stressful conditions (Koren et al., 2002; Davenport et al., 2006; Accorsi et al., 2008; Macbeth et al., 2010; Comin et al., 2011; Fairhurst et al., 2014).”
Background
Male-inflicted wounds have opposite effects on hair cortisol for captive male and female rhesus macaques (Macaca mulatta) following new group formation
Linden, J. B., McCowan, B., Capitanio, J. P., & Isbell, L. A. (2018) · Primates · doi:10.1007/s10329-018-0703-6 · Cited by 14
Is the Implicit Association Test for Aggressive Attitudes a Measure for Attraction to Violence or Traumatization?
Bluemke, M., Crombach, A., Hecker, T., Schalinski, I., Elbert, T. R., & Weierstall, R. (2017) · Zeitschrift für Psychologie · doi:10.1027/2151-2604/a000281 · Cited by 14
A Procedure for Oxytocin Measurement in Hair of Pig: Analytical Validation and a Pilot Application
López-Arjona, M., Tecles, F., Mateo, S. V., Contreras-Aguilar, M. D., Martínez-Miró, S., Cerón, J. M. C., & Martı́nez-Subiela, S. (2021) · Biology · doi:10.3390/biology10060527 · Cited by 13
Moderated Online Social Therapy for Carers of Early Psychosis Clients in Real-World Settings: Cluster Randomized Controlled Trial
Gleeson, J., Lin, A. P., Koval, P., Hopkins, L., Denborough, P., Lederman, R., Herrman, H., Bendall, S., Eleftheriadis, D., Cotton, S., et al. (2023) · JMIR Mental Health · doi:10.2196/47722 · Cited by 15
“The hair cortisol analysis procedures included repeated washing of hair samples with isopropanol, drying, weighing (weight: 7.5, SD 0.5 mg), steroid extraction with methanol, evaporation of methanol (at 50 °C), and cortisol determination [27].”
BackgroundMethodInfluential
Longitudinal hair cortisol in bipolar disorder and a mechanism based on HPA dynamics
Milo, T., Maimon, L., Cohen, B., Haran, D., Segman, D., Danon, T., Bren, A., Mayo, A., Rappaport, G. C., McInnis, M. G., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109234 · Cited by 16
“To measure cortisol we used hair, because it offers advantages over other assays, namely blood, saliva and urine measurements (D’Anna-Hernandez et al. 2011; Davenport et al. 2006; Mayer et al. 2019; Sauvé et al. 2007).”
Method
Hair cortisol level might be indicative for a 3PM approach towards suicide risk assessment in depression: comparative analysis of mentally stable and depressed individuals versus individuals after completing suicide
Karabatsiakis, A., de Punder, K., Salinas-Manrique, J., Todt, M., & Dietrich, D. E. (2022) · The EPMA Journal · doi:10.1007/s13167-022-00296-z · Cited by 18
“For the pre-analytical processing and isopropanol washing of samples, we performed the protocol given by Davenport and colleagues (2006) [64].”
Method
Associations between skin lesion counts, hair cortisol concentrations and reproductive performance in group housed sows
Lagoda, M. E., O’Driscoll, K., Marchewka, J., Foister, S., Turner, S. P., & Boyle, L. A. (2021) · Livestock Science · doi:10.1016/j.livsci.2021.104463 · Cited by 13
Landscape of stress: Tree mortality influences physiological stress and survival in a native mesocarnivore
Kordosky, J., Gese, E. M., Thompson, C. M., Terletzky, P. A., Neuman‐Lee, L. A., Schneiderman, J. D., Purcell, K. L., & French, S. S. (2021) · PLoS ONE · doi:10.1371/journal.pone.0253604 · Cited by 12
Hair cortisol concentration associates with insomnia and stress symptoms in breast cancer survivors
Ahabrach, H., Mlili, N. E., Mafla-España, M. A., & Cauli, O. (2023) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2023.07.006 · Cited by 12
Prenatal family income, but not parental education, is associated with resting brain activity in 1-month-old infants
Sandre, A., Troller‐Renfree, S. V., Giebler, M. A., Meyer, J. S., & Noble, K. G. (2024) · Scientific Reports · doi:10.1038/s41598-024-64498-3 · Cited by 12
Application of Felid Hair for Non-Invasive Tracking of Animal Reproductive Status and Adrenal Activity
Naidenko, S. V., Alekseeva, G. S., Klyuchnikova, P. S., & Erofeeva, M. (2022) · Animals · doi:10.3390/ani12202792 · Cited by 12
“The correlations of the level of hair cortisol with the feces [19] or saliva [20] cortisol concentrations suggest that steroid hormones become present in hairs soon after their level increases in the blood stream [12].”
Background
Assessment of Chronic Stress: Comparison of Hair Biomarkers and Allostatic Load Indices
Wippert, P., Honold, J., Wang, V., & Kirschbaum, C. (2014) · Journal of Psychology Research · doi:10.17265/2159-5542/2014.07.001 · Cited by 12
Measurement of cortisol, dehydroepiandrosterone, and testosterone in the hair of children: Preliminary results and promising indications
Smith, J., Johnson, K. A., Whittle, S., Allen, N. B., & Simmons, J. G. (2018) · Developmental Psychobiology · doi:10.1002/dev.21807 · Cited by 12
Pre-pandemic socio-emotional vulnerability, internalizing and externalizing symptoms predict changes in hair cortisol concentrations in reaction to the COVID-19 pandemic in children
Raymond, C., Bilodeau-Houle, A., Zerroug, Y., Provencher, J., Beaudin, M., & Marin, M. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105888 · Cited by 13
Differential relationships between chronic hormone profiles in pregnancy and maternal investment in rhesus monkey mothers with hair loss in the neonatal period
Dettmer, A. M., Rosenberg, K. L., Menard, M. T., El‐Mallah, S. N., Woodward, R. A., Suomi, S. J., & Meyer, J. S. (2015) · American Journal of Primatology · doi:10.1002/ajp.22489 · Cited by 12
“…in these samples reflected chronic steroid deposition over the previous time period (specifically three months in the case of the July and October samples; and 3–6 months for the April sample, as the monkeys were shaved in October 2012 and in April, July, and October 2013) [Davenport et al., 2006].”
Savanna Monkeys
Turner, T. R., Schmitt, C. A., & Cramer, J. D. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139019941 · Cited by 18
Unraveling the Complexity to Observe Associations Between Welfare Indicators and Hair Cortisol Concentration in Dairy Calves
Tamminen, L., Keeling, L. J., Svensson, A. C., Briot, L., & Emanuelson, U. (2021) · Frontiers in Animal Science · doi:10.3389/fanim.2021.793558 · Cited by 11
Cortisol in Hair: Do Habitat Fragmentation and Competition with Golden Jackal (Canis aureus) Measurably Affect the Long-Term Physiological Response in European Wildcat (Felis silvestris)?
Filacorda, S., Comin, A., Franchini, M., Frangini, L., Pesaro, S., Pezzin, E. N., & Prandi, A. (2021) · Annales Zoologici Fennici · doi:10.5735/086.059.0101 · Cited by 11
“In fact, GCs accumulate in such a medium for an extended period, varying from weeks to years depending on the hair length (Davenport et al. 2006, Macbeth et al. 2010, Meyer & Novak 2012).”
Background
Hair as an alternative noninvasive matrix: sources of variation in testosterone levels
Calamari, C. V., Viau, P., Nichi, M., Martins, G. S., Sobral, G., Dias, J. H. M., & de Oliveira, C. A. (2020) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2020.106477 · Cited by 11
Inter- and intra-specific variation in hair cortisol concentrations of Neotropical bats
Herrera, N. S., Mastromonaco, G. F., Becker, D. J., Simmons, N. B., & Welch, K. C. (2021) · Conservation Physiology · doi:10.1093/conphys/coab053 · Cited by 11
Alopecia in rhesus macaques (Macaca mulatta): Association with pregnancy and chronic stress
Lutz, C. K., Menard, M. T., Rosenberg, K. L., Meyer, J. S., & Novak, M. A. (2019) · Journal of Medical Primatology · doi:10.1111/jmp.12419 · Cited by 11
Hierarchy Establishment in Growing Finishing Pigs: Impacts on Behavior, Growth Performance, and Physiological Parameters
de Oliveira, A. C. D. F., Wéber, H., Ramayo‐Caldas, Y., Dalmau, A., & Costa, L. B. (2023) · Animals · doi:10.3390/ani13020292 · Cited by 10
“Cortisol extraction was conducted following the method of [38].”
Method
Is Smart Working Beneficial for Workers’ Wellbeing? A Longitudinal Investigation of Smart Working, Workload, and Hair Cortisol/Dehydroepiandrosterone Sulfate during the COVID-19 Pandemic
Falco, A., Girardi, D., Elfering, A., Peric, T., Pividori, I., & Corso, L. D. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20136220 · Cited by 12
Homogeneous immunoassay of cortisol based on microchip electrophoresis with chemiluminescence detection
Ye, F., Yang, T., Huang, Y. X., Li, S., & Zhao, S. (2013) · Analytical Methods · doi:10.1039/c3ay40949j · Cited by 10
A novel and innovative hair test to determine glucocorticoid levels in racing camels for use in assessment of doping, health, and disease
Shah, I., Haddow, J. D., Ibrahim, H. A., Sheikh, M. V. A., & Alhemeiri, F. S. A. (2017) · Drug Testing and Analysis · doi:10.1002/dta.2311 · Cited by 10
Hair cortisol levels and symptoms of anxiety and depression in Chinese adolescents: Comparison between incarcerated and community populations
Xu, Y., Li, J., Xie, Q., & Deng, H. (2018) · PsyCh Journal · doi:10.1002/pchj.248 · Cited by 11
Hair cortisol concentration in veal calves reared under two different welfare production labels
Braun, U., Wiest, A., Lutz, T. A., Riond, B., Stirn, M., Hilbe, M., Baumgartner, M. R., & Binz, T. M. (2019) · Research in Veterinary Science · doi:10.1016/j.rvsc.2019.01.027 · Cited by 10
Direct sunlight exposure reduces hair cortisol levels in rhesus monkeys (Macaca mulatta)
Feng, X., Che, H.-L., Xi-Ning, Ba, X.-Y., Li, J., Zhang, J., Wang, Y., Hu, Z., Hu, X., & Ren, X. (2019) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2019.064 · Cited by 10
“It can reflect cumulative cortisol levels in an organism over a 3–5-month period and is thus suitable for measuring the long-term cumulative levels of cortisol (Davenport et al., 2006; Kalra et al., 2007).”
Background
Diurnal Variation in Peripheral (Hair) vs Central (Saliva) HPA Axis Cortisol Concentrations
Sharpley, C. F., Kauter, K., & McFarlane, J. R. (2010) · Clinical Medicine Insights Endocrinology and Diabetes · doi:10.4137/cmed.s4350 · Cited by 10

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.
ORCID: Lutz, Corrine K.
Novak, Melinda A.
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)
DOI: 10.1016/j.ygcen.2006.01.005
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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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Analysis of endogenous cortisol concentrations in the hair of rhesus macaques

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