Comparative Aspects of the Metabolism and Excretion of Cortisol in Three Individual Nonhuman Primates
Abstract
A radiometabolism study is described to provide the first comparative data on the time course, route, and characteristics of excreted [3H]cortisol metabolites in three nonhuman primates: the common marmoset (Callithrix jacchus), the long-tailed macaque (Macacafascicularis), and the chimpanzee (Pan troglodytes). A low dose (40-100 microCi) of 3H-labeled cortisol was administered intravenously to one adult male of each species and the excreta collected over a 5-day period postinjection. The major proportion of radioactivity was excreted in the urine (>80%). Peak radioactivity in urine was recovered within 5.5 h following injection in all three species, while in the feces peak levels of radioactivity were recovered within 26 h postinjection. In all three species, urinary metabolites were primarily excreted as conjugates (61-87%), whereas the percentage of conjugated metabolites in feces was 50% or less. The number and relative abundance of urinary and fecal [3H]cortisol metabolites were determined by reverse-phase high-performance liquid chromatography (HPLC) and immunoreactivity of the radioactivity peaks was assessed by screening HPLC fractions with established cortisol, corticosterone, and 11-oxoetiocholanolone enzyme immunoassays (EIA), the latter being a group-specific assay for measuring 11,17-dioxoandrostanes. HPLC separation of urinary and fecal extracts revealed multiple peaks of radioactivity, several of which were common to all three species. The relative proportion of these peaks, however, differed considerably among species and between urine and feces. HPLC indicated that native cortisol was a major urinary excretory product in the marmoset, while comparatively small amounts were present in the urine of the macaque and chimpanzee. In contrast, in feces, cortisol was only detected in low amounts in the marmoset and was virtually absent in the macaque and chimpanzee. In all three species, one of the major radioactivity peaks showed a retention time comparable to 11-oxoetiocholanolone and high immunoreactivity in the 11-oxoetiocholanolone EIA. The measurement of urinary- and/or fecal-immunoreactive 11,17-dioxoandrostanes is therefore implicated for noninvasive assessment of adrenal function in Old World monkeys, New World monkeys, and great apes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Creatinine levels were measured in all urine samples and urinary oxytocin values were expressed as pg/mg creatinine, to control for variation in urine volume and concentration.
“We measured creatinine levels in all urine samples and expressed urinary oxytocin values as pg/mg creatinine, to control for variation in urine volume and concentration (44).”
From Oxytocin reactivity during intergroup conflict in wild chimpanzees (2017) · cites this paper as [44]
To compensate for variation in urine concentration, creatinine levels were measured in each sample and all oxytocin values were expressed as pg mg−1 crea.
“To compensate for variation in urine concentration, we measured creatinine (crea) levels in each sample [66] and expressed all oxytocin values as pg mg 21 crea.”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [66]
Cites
Palme, R., & Moestl, E. (1997) · Cited by 525 · see citing works
Self-citationEstrogen excretion patterns and plasma levels in vegetarian and omnivorous women
Goldin, B. R., Adlercreutz, H., Gorbach, S. L., Warram, J. H., Dwyer, J. T., Swenson, L., & Woods, M. N. (1982) · New England Journal of Medicine · doi:10.1056/nejm198212163072502 · Cited by 474 · see citing works
Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock
Palme, R., Fischer, P., Schildorfer, H., & Ismail, M. N. (1996) · Animal Reproduction Science · doi:10.1016/0378-4320(95)01458-6 · Cited by 410 · see citing works
Self-citationSchwarzenberger, F., Möstl, E., Palme, R., & Bamberg, E. (1996) · Animal Reproduction Science · doi:10.1016/0378-4320(96)01561-8 · Cited by 389 · see citing works
Self-citationCavigelli, S. A. (1999) · Animal Behaviour · doi:10.1006/anbe.1998.1054 · Cited by 275 · see citing works
Wasser, S. K., Monfort, S. L., Southers, J. L., & Wildt, D. E. (1994) · Reproduction · doi:10.1530/jrf.0.1010213 · Cited by 224 · see citing works
Wasser, S. K., Thomas, R., Nair, P. P., et al. (1993) · Reproduction · doi:10.1530/jrf.0.0970569 · Cited by 218 · see citing works
Graham, L. H., & Brown, J. L. (1996) · Zoo Biology · doi:10.1002/(sici)1098-2361(1996)15:1 · Cited by 185 · see citing works
Strier, K. B., Ziegler, T. E., & Wittwer, D. J. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1998.1505 · Cited by 177 · see citing works
Stress, social status, and reproductive physiology in free-living baboons.
Sapolsky, R. M. (1987) · Cited by 167 · see citing works
Social and reproductive influences on plasma cortisol in female marmoset monkeys
Wendy Saltzman, A., SCHULTZ‐DARKEN, N. J., Scheffler, G., Wegner, F. H., & Abbott, D. H. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90246-1 · Cited by 154 · see citing works
Shideler, S. E., Ortuño, A. M., Moran, F. M., et al. (1993) · Biology of Reproduction · doi:10.1095/biolreprod48.6.1290 · Cited by 153 · see citing works
Milton, K., & Demment, M. W. (1988) · Journal of Nutrition · doi:10.1093/jn/118.9.1082 · Cited by 149 · see citing works
Psychosocial Stress and Urinary Cortisol Excretion in Marmoset Monkeys
SMITH, T., & French, J. A. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00103-0 · Cited by 143 · see citing works
Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes)
Whitten, P. L., Stavisky, R. C., Aureli, F., & Russell, E. (1998) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1998)44:1 · Cited by 138 · see citing works
Johnson, E. O., Kamilaris, T. C., Carter, C. S., Calogero, A. E., Gold, P. W., & Chrousos, G. P. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00397-5 · Cited by 132 · see citing works
Crockett, C. M., Bowers, C. L., Sackett, G. P., & Bowden, D. M. (1993) · American Journal of Primatology · doi:10.1002/ajp.1350300105 · Cited by 111 · see citing works
Physiology of Urinary Cortisol Excretion
Beisel, W. R., COS, J. J., Horton, R., Chao, P. Y., & Forsham, P. H. (1964) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-24-9-887 · Cited by 108 · see citing works
Evaluating adrenal activity in African wild dogs (Lycaon pictus) by fecal corticosteroid analysis.
Monfort, S. L., Mashburn, K. L., Brewer, B. A., et al. (1998) · PubMed · Cited by 108 · see citing works
Physiologic basis and consequences of distress in animals
Breazile, J. E. (1987) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.1987.191.10.1212 · Cited by 107 · see citing works
Immunopharmacology and the regulation of leukocyte function
(1983) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(83)90124-6 · Cited by 102 · see citing works
Stress and Behaviorally Induced Reproductive Dysfunction in Primates
Cameron, J. (1997) · Seminars in Reproductive Endocrinology · doi:10.1055/s-2008-1067966 · Cited by 102 · see citing works
Bahr, N. I., Pryce, C. R., Döbeli, M., & Martin, R. D. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00057-2 · Cited by 101 · see citing works
Self-citationZiegler, T. E., Sholl, S. A., Scheffler, G., et al. (1989) · American Journal of Primatology · doi:10.1002/ajp.1350170302 · Cited by 82 · see citing works
Peterson, J. I. (1969) · Analytical Biochemistry · doi:10.1016/0003-2697(69)90258-9 · Cited by 73 · see citing works
Fecal Glucocorticoids Document Stress in Female Barbary Macaques (Macaca sylvanus)
Wallner, B., Möstl, E., Dittami, J., & Prossinger, H. (1999) · General and Comparative Endocrinology · doi:10.1006/gcen.1998.7183 · Cited by 64 · see citing works
Kalin, N. H., & Shelton, S. E. (1998) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1998)44:2 · Cited by 56 · see citing works
Heistermann, M., Agil, M., Büthe, A., et al. (1998) · Animal Reproduction Science · doi:10.1016/s0378-4320(98)00111-0 · Cited by 43 · see citing works
Self-citationNorman, R. L. (1993) · Biology of Reproduction · doi:10.1095/biolreprod49.1.148 · Cited by 42 · see citing works
Excretion of radiolabeled estradiol metabolites in the slow loris (Nycticebus coucang)
Perez, L. E., Czekala, N. M., Weisenseel, K. A., & Lasley, B. L. (1988) · American Journal of Primatology · doi:10.1002/ajp.1350160404 · Cited by 36 · see citing works
EFFECT OF STRESS ON THE PROFILE OF PLASMA STEROIDS IN BABOONS (PAPIO HAMADRYAS)
Goncharov, N. P., Taranov, A. G., Antonichev, A. V., Gorlushkin, V. M., Asô, T., Cekan, S. Z., & Diczfalusy, E. R. (1979) · European Journal of Endocrinology · doi:10.1530/acta.0.0900372 · Cited by 35 · see citing works
“Environmental stress” and reproductive success in the common marmoset (Callithrix jacchus jacchus)
Johnson, E. O., Kamilaris, T. C., Carter, C. S., Gold, P. W., & Chrousos, G. P. (1991) · American Journal of Primatology · doi:10.1002/ajp.1350250306 · Cited by 32 · see citing works
15th International Symposium on Column Liquid Chromatography
(1991) · Analytical Chemistry · doi:10.1021/ac00009a721 · Cited by 17 · see citing works
The secretion rate of cortisol in immature chimpanzees
Layne, D. S., Kirdani, R. Y., Gleason, T., et al. (1964) · General and Comparative Endocrinology · doi:10.1016/0016-6480(64)90048-6 · Cited by 12 · see citing works
Advances in steroid analysis '90
(1991) · Analytica Chimica Acta · doi:10.1016/0003-2670(91)90043-5 · Cited by 12 · see citing works
Measuring Gut Passage Times in Small New World Monkeys
Price, E. C. (1993) · Animal Welfare · doi:10.1017/s0962728600016122 · Cited by 6 · see citing works
Nash, L. (1999) · doi:10.1002/(sici)1098-2345(1999)48:1
Flagged first, then by citations
Cited by
Sorted by citations
Touma, C., Sachser, N., Möstl, E., & Palme, R. (2003) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(02)00620-2 · Cited by 581 · see citing works
Self-citationWittig, R. M., Crockford, C., Deschner, T., Langergraber, K. E., Ziegler, T. E., & Zuberbühler, K. (2014) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2013.3096 · Cited by 235 · see citing works
Oxytocin reactivity during intergroup conflict in wild chimpanzees
Samuni, L., Preis, A., Mundry, R., Deschner, T., Crockford, C., & Wittig, R. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616812114 · Cited by 207 · see citing works
Evidence that zoo visitors influence HPA activity in spider monkeys (Ateles geoffroyii rufiventris)
Davis, N., Schaffner, C. M., & Smith, T. E. (2005) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.08.020 · Cited by 128 · see citing works
Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys
Cavanaugh, J., Carp, S. B., Rock, C. M., & French, J. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.12.027 · Cited by 64 · see citing works
Territoriality, tolerance and testosterone in wild chimpanzees
Sobolewski, M. E., Brown, J. L., & Mitani, J. C. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.09.018 · Cited by 55 · see citing works
- Authors
- Bahr, N. I., Palme, R., Möhle, U., Hodges, J. K., & Heistermann, M.
- Affiliations
- German Primate Center (DE)
- University of Veterinary Medicine Vienna (AT)
- Corresponding author
- Heistermann, M.
- ORCID
- Palme, R.
- Venue
- General and Comparative Endocrinology
- Publisher
- Elsevier BV
- Published
- 2000-03
- Volume
- 117
- Issue
- 3
- Pages
- 427-438
- ISSN
- 0016-6480 (ISSN-L)
- OpenAlex
- W2091531784
- Cited by
- 270
- References
- 37
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 6 · 2023: 12 · 2022: 8 · 2021: 13 · 2020: 14 · 2019: 12 · 2018: 16 · 2017: 20 · 2016: 12 · 2015: 15 · 2014: 12 · 2013: 11 · 2012: 16
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- General and Comparative Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacogenetics and Drug Metabolism
- Keywords
- cortisol metabolism, cortisol excretion, urinary cortisol, fecal cortisol, corticosterone, non-human primates, Callithrix jacchus, Macaca fascicularis, chimpanzees, species comparison, radiometabolism
- MeSH terms
- Animals, Callithrix, Pan troglodytes, Chromatography, High Pressure Liquid, Corticosterone, Etiocholanolone, Feces, Hydrocortisone, Immunoenzyme Techniques, Kinetics, Macaca fascicularis, Male, Tritium
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review