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. Author manuscript; available in PMC: 2025 Apr 1.
Published in final edited form as: Am J Primatol. 2024 Jan 18;86(4):e23597. doi: 10.1002/ajp.23597

Cortisol Levels Across the Lifespan in Common Marmosets (Callithrix jacchus)

Matthew Lopez 1, Amaya Siedl 1, Kimberley A Phillips 1,2
PMCID: PMC10959686  NIHMSID: NIHMS1956042  PMID: 38239052

Abstract

Human aging is associated with senescence of the hypothalamic-pituitary-adrenal (HPA) axis, leading to progressive dysregulation characterized by increased cortisol exposure. This key hormone is implicated in the pathogenesis of many age-related diseases. Common marmosets (Callithrix jacchus) display a wide spectrum of naturally-occurring age-related pathologies that compare similarly to humans, and are increasingly used as translational models of aging and age-related disease. Whether the marmoset HPA axis also shows senescence with increasing age is unknown. We analyzed hair cortisol concentration (HCC) across the lifespan of 50 captive common marmosets, ranging in age from approximately 2 months – 14.5 years, via a cross-sectional design. Samples were processed and analyzed for cortisol using enzyme immunoassay. HCC ranged from 1,416 to 15,343 pg/mg and was negatively correlated with age. We found significant main effects of age group (infant, adolescent, adult, aged, very aged) and sex on HCC, and no interaction effects. Infants had significantly higher levels of HCC compared to all other age groups. Females had higher HCC than males. There was no interaction between age and sex. These results suggest marmosets do not show dysregulation of the HPA axis with increasing age, as measured via HCC.

Keywords: Glucocorticoids, Aging, nonhuman primates, common marmoset

Graphical Abstract

graphic file with name nihms-1956042-f0001.jpg

Marmosets display age-related changes in hair cortisol concetration (HCC) across the lifespan, with HCC significantly decreasing from infancy to adolescence and remaining consistent throughout the restof the lifespan.

1. Introduction

Glucocorticoids are steroid hormones involved in essential physiological processes, including metabolism (Vegiopoulos & Herzig, 2007), water and electrolyte balance (Hawkins et al., 2012), immune response (Cruz-Topete & Cidlowski, 2015), mood and cognitive functions (Farrell & O’Keane, 2016; Tatomir et al., 2014), and cardiovascular function (Cruz-Topete et al., 2016). Adrenal glucocorticoids are regulated by the hypothalamic-pituitary-adrenal (HPA) axis. Under basal conditions, glucocorticoids are released into the bloodstream in a circadian and ultradian rhythm, with peak levels during the morning in humans. When the HPA axis is stimulated due to physiological or psychological stress, glucocorticoid synthesis and secretion increases.

While a swift stress response via the HPA axis is a crucial survival mechanism, timely downregulation is important to avoid the negative effects of glucocorticoid excess. Chronic exposure to stress leads to overactivity of the HPA axis, amplifying long-term glucocorticoid levels and triggering widespread consequences, increasing the risk of psychological, cardiovascular, and immune pathologies rooted in chronic HPA axis dysregulation. High glucocorticoid levels are associated with obesity, osteoporosis, hypertension, and diabetes mellitus (Baid & Nieman, 2004; Bjorntorp & Rosmond, 2000; Manelli & Giustina, 2000; Suh & Park, 2017). Furthermore, glucocorticoids, particularly cortisol, have been implicated in a variety of pathophysiologies associated with aging in humans (Gardner et al., 2013), including late-life depression and anxiety (Piazza et al., 2010), dementia of degenerative and vascular origins (Balldin et al., 1983), cardiovascular disease (Iob & Steptoe, 2019), and mortality risk (Schoorlemmer et al., 2009). In humans, senescence of the HPA axis leads to progressive dysregulation, which is marked by sustained elevated glucocorticoid production and exposure (Moffat et al., 2020). A cross-sectional study in humans reported cortisol concentration increased with age (Feller et al., 2014).

Cortisol can be measured from blood, saliva, urine, feces, and hair; each of these provides insight into a different time frame of the sample. Cortisol obtained from blood and saliva are understood to provide “point” measures, as the measurement indicates a time frame of minutes since the cortisol was excreted (J. Meyer & M. Novak, 2012). Urine and feces are considered “state” measures and reflect activity of the HPA axis over several hours up to a few days (J. S. Meyer & M. A. Novak, 2012). Long-term HPA axis activity over weeks or months, depending upon the length of hair analyzed, can be quantified via analysis of hair cortisol content (Davenport et al., 2006).

Research into the relationships between HCC and sex has revealed no consistent pattern across primate species. Females were reported to have higher HCC than males in baboons (Papio hamadryas anubis: (Lutz et al., 2021), common marmosets (Garber et al., 2020), rhesus macaques (Macaca mulatta; (Dettmer et al., 2014), and vervet monkeys ((Laudenschlager et al., 2012); males showed higher HCC than females in humans (Dettenborn et al., 2012); and other studies have reported no sex differences (common marmosets (Phillips et al., 2018), chimpanzees (Pan troglodytes: (Yamanashi et al., 2013), orangutans (Pongo spp.: (Carlitz et al., 2014), Tonkean macaques (Macaca tonkeana), and long-tailed macaques (Macaca fascicularis: (Sadoughi et al., 2021).

Although studies on aging of the HPA axis in non-human primates are limited, many species display age-related declines in cortisol concentration [rhesus macaques (Macaca mulatta), vervet monkeys (Chlorocebus aethiops), and baboons (Papio hamadryas)], as measured via plasma and hair (Dettmer et al., 2014; Fourie & Bernstein, 2011; Goncharova & Lapin, 2004; Lutz et al., 2021). While these studies generally have not included aged or geriatric subjects, a recent longitudinal study examined age-related changes in cortisol levels in wild chimpanzees ranging from approximately 10 – 63 years (Emery Thompson et al., 2020). Urinary cortisol displayed significant increases with age in these chimpanzees. In humans, Dettenborn et al. (2012) reported elevated HCC in young children and older adults.

Nonhuman primates are critical biomedical models, including the areas of geroscience and the translation of the basic biology of aging to clinical applications. Common marmosets (Callithrix jacchus) have recently emerged as a valuable model for the study of aging and age-related diseases (Ross, 2019; Tardif et al., 2011). In addition to their small size and compatibility with laboratory housing in species-typical social groups, the marmoset is the fastest developing anthropoid primate, reaching sexual maturity by 2 years of age. Marmosets are considered aged around 7 years, and very aged or geriatric at around 10 years (Geula et al., 2002; Ross, 2019). Marmosets have been found to display many aging phenotypes that mimic human aging, including increased risk of cardiovascular changes, inflammatory disease, metabolic impairment, suppressed immune function, and impaired cognition (Ross, 2019; Ross et al., 2019; Ross et al., 2012).

Our previous work with marmosets demonstrated sex and age differences in hair cortisol concentration (HCC), with females presenting higher HCC than males, and juveniles presenting higher HCC than adults (Garber et al., 2020). However, there has not been an examination of HCC across the lifespan in common marmosets. Notably, few studies have studied cortisol across the lifespan in any primate species, choosing instead to focus on cortisol within certain period of life, such as infancy or adulthood. Here, we conducted a cross-sectional study to investigate age-related changes in HCC in common marmosets. We sampled individuals ranging in age from 2 weeks (infancy) to 14.5 years (very aged). As infant marmosets are known to exhibit hypercortisolism, we were particularly interested in determining whether marmosets exhibit senescence of the HPA axis, as indicated by an increase in HCC during the geriatric stages.

2. Methods

2.1. Animals

Our sample consisted of 50 common marmosets (Callithrix jacchus; male n = 25, female n = 25) ranging in age from 2.5 weeks through 14.5 years. These marmosets came from five age groups: infant, adolescent, adult, aged, and very aged (Ross et al., 2012, 2019; Tardif, 2019). The infant category included the youngest animals between birth and 3-months of age. Adolescent included those animals that are still growing and maturing, and included animals in the 12-month to 18-month range. Adult individuals are sexually mature. We restricted the adult sample to individuals between 3 and 5 years. Aged animals are those that are beginning to display an aged phenotype and included animals between 7–9 years. Very aged animals, those > 10 years, are considered fully geriatric and fully exhibit the aged phenotype (Ross et al., 2012, 2019). Five males and five females were sampled from each age group. All animals were socially housed except one adult male and one adult female during the three months prior to hair collection. Infants, adolescents, and two adult male breeders were kept in their family groups at the time of collection. Subjects were housed at the Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX, USA and maintained in accordance with the Guide for the Care and Use of Laboratory Animals (ILAR, 2011). Room temperatures were maintained at 81–91°F (27–33°C) and a 12h:12h light: dark cycle. Marmosets had fresh food ad libitum which consisted of a purified diet (Harlan Teklad TD130059 PWD) and Mazuri diet (AVP Callitrichid 5LK6), supplemented with fresh fruits, vegetables, seeds, and cottage cheese. The research adhered to the American Society of Primatologists Principles for the Ethical Treatment of Non-Human Primates.

2.2. Sample collection

Research staff collected approximately 100g of hair from the upper back of each animal using an electric shaver. Samples were opportunistically collected during routine health screenings. The electric shaver was cleaned with disinfectant after each use. Samples were stored at room temperature, out of direct sunlight, in paper envelopes until processed and analyzed.

2.3. Cortisol assay

We used a previously validated procedure to extract and assay cortisol from marmoset hair (Meyer et al., 2014; Phillips et al., 2018). A step-by-step protocol for the extraction and assay procedure has been deposited at the protocols.io repository (dx.doi.org/10.17504/protocols.io.bw8wphxe). We analyzed 0.5 cm of hair from the proximal end of the sample. Marmoset samples were diluted 1:40 with phosphate buffer solution before being analyzed, in duplicate, using a commercially available enzyme immunoassay kit (Salimetrics, State College, PA). Resulting values, expressed as μg/dL, were converted into pg/mg for analysis.

2.4. Data analysis

All analyses were performed using R Statistical Software (v4.0.2; R Core Team, 2020). Intraassay coefficient of variation (CV) was 3% and the interassay CV was 5.3%. One subject, a male infant, was determined to be unhealthy from test results obtained during the health screening; thus, that animal’s hair sample was excluded from analysis. Therefore, there were 9 animals (male n=4, female n=5) in the infant age group. We performed the Shapiro-Wilks test of normality for HCC concentration within each age group before statistical analysis. As this indicated HCC within age groups were normally distributed, we conducted a two-way analysis of variance, testing for main effects of sex and age group, and an interaction effect. We also performed correlational analysis on the HCC values and age (in months). Alpha was set at 0.05.

3. Results

We analyzed hair cortisol concentration (HCC) via enzyme immunoassay in 49 captive common marmosets divided into five age groups spanning the entire lifespan. Overall, HCC in our sample of common marmosets ranged from 1,416 to 15,343 pg/mg. An analysis of variance showed a main effect of age group, F(4, 39) = 17.32, p < 0.001 (Figure 1). Post hoc analyses using the Bonferroni criterion for significance indicated that infants had significantly higher HCC compared to all other age groups. No other pairwise comparisons were significant. Additionally, a main effect of sex was found, F(1, 39) = 4.66, p = 0.037, with females having higher HCC than males. The interaction between sex and age group was not significant.

Figure 1.

Figure 1.

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The distribution of hair cortisol concentration in each age group, showing the mean and standard error of the mean.

HCC displayed a moderate negative correlation with animal age (in months), r(47) = 0.51, p < 0.05 (Figure 2). Examination of these data revealed large variation in HCC within the infant group in comparison to those of other age groups, leading us to question whether survival was related to HCC in infancy. As all of these infants survived to 9 months of age, we did not find survival to be associated with HCC.

Figure 2.

Figure 2.

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The association between hair cortisol concentration (HCC) and age in common marmosets. HCC showed a moderate, negative correlation with age (in months), r(47) = 0.51, p < 0.05.

4. Discussion

Our results indicate marmosets display age-related changes in HCC across the lifespan, with HCC decreasing significantly from the infant to adolescent stage and remaining low throughout adult, aged, and very aged age groups. We also found a significant effect of sex, with females having higher HCC than males. We did not detect an interaction between sex and age group.

Our data support hypercortisolism in infants brought on by postnatal HPA hyperactivity and a suppression of the negative glucocorticoid feedback system. High circulating glucocorticoid levels in infancy followed by sharp decline is well established in marmosets (Pryce et al., 2002) as well as baboons (Gesquiere et al., 2005), and demonstrated among many platyrrhine taxa (i.e. Central and South American monkeys) (Fourie & Bernstein, 2011). Certain platyrrhines exhibit glucocorticoid resistance arising from varying glucocorticoid receptor binding affinities that influence circulating hormone levels, which may contribute to differing long standing patterns between species (Pryce et al., 2002). These distinctions in endocrine physiology position the common marmoset as a model for evaluating long-term consequences of high postnatal glucocorticoid exposure and identifying developmental distinctions across species in the hypothalamic system.

We found HCC to be negatively correlated with age, and we did not detect an increase in HCC in aged or very aged marmosets. This pattern of declining cortisol from young to adult ages has been reported in numerous species, including vervet monkeys (Chlorocebus aethiops), rhesus monkeys (Macaca mulatta), baboons (Papio spp.) (Dettmer et al., 2014; Fourie & Bernstein, 2011; Laudenslager et al., 2012). Studies examining cortisol trends across the human lifespan have shown mixed results. While some demonstrate increases in basal cortisol production with age (Moffat et al., 2020; Nicolson et al., 1997; Pavlov et al., 1986), others only demonstrate increased HPA axis responsiveness or diminished negative feedback control (Born et al., 1995; Otte et al., 2005; Rohleder et al., 2003). To date, among nonhuman primates only chimpanzees have been found to show senescence of the HPA axis (Emery Thompson et al., 2020). This study found a significant increase in urinary cortisol in adult wild chimpanzees over a period of 20 years, suggesting that increasing cortisol concentrations may be an aspect of the normal aging process in chimpanzees.

Our finding of female common marmosets having higher HCC than males is consistent with Garber et al. (2020)’s investigation of HCC in wild common marmosets, yet differs from a study in captive common marmosets which reported no sex differences (Phillips et al., 2018). Other nonhuman primate species also show sex differences in HCC, though the influence of sex on cortisol is inconsistent. Numerous factors influence HCC, including sex, age, body condition and nutritional status, diseases and disorders, season (Heimburge et al., 2019), and differential metabolism of gonadal steroids among males and females (Laudenschlager et al., 2012). For example, in some macaque species, sex differences in HCC are influenced by social status and social organization (Sadoughi et al., 2021; Vandeleest et al., 2020).

Two characteristics of the present study and their potential effects on our results should be noted: 1) we utilized a cross-sectional design to investigate cortisol concentration across age groups; and 2) we assayed cortisol via a state measure (hair) rather than a point measure (e.g., serum or urine). While previous studies on humans and nonhuman primates utilizing cross-sectional designs have reported similar findings of cortisol concentration decreasing with age (Feldman et al., 2002; Lutz et al., 2021), Feller et al. (2014) and Nicolson et al. (1997) found HCC to be positively correlated with age in humans. Some longitudinal approaches have reported a different association of cortisol with age. Moffat et al. (2020), using a longitudinal approach to study cortisol changes across the lifespan in humans, reported sustained elevated increased glucocorticoid concentrations. Additionally, Emery Thompson et al. (2020) reported similar findings in a longitudinal study of adult wild chimpanzees. Thus, it is feasible that longitudinal study would reveal different age-related patterns of HCC in marmosets. A second consideration concerns our use of hair to evaluate cortisol concentration instead of urine, which is how Moffat et al. 2020 and Emery Thompson et al. 2020 assayed cortisol. HCC is regularly used as a noninvasive measure to assess retrospective HPA axis activity (Heimburge et al. 2019) and provides an index of long-term systemic cortisol concentration. HPA axis activity demonstrates high variability, impacted by factors such as circadian rhythmicity, acute stress, and food intake. Consequently, acute cortisol levels (those obtained from urinary, blood or saliva samples) reflect the acute context of when the sample was obtained and may not be the best indicator of long-term cortisol secretion. A longitudinal study of cortisol utilizing HCC is needed to fully understand how age-related patterns of HCC.

Considering the differing findings in human and nonhuman primate investigations into cortisol concentrations with respect to age, it seems plausible that senescence of the HPA axis may not be characteristic or an inevitable consequence of aging, but rather may arise in certain populations due to variation in life course. Numerous studies have demonstrated individual variations in cortisol concentration trajectories, and these differences are associated with cognitive decline trends (Ennis et al., 2017; Lupien et al., 1994). For example, Franz et al. (2011) reported a significant association between cortisol levels and cognition in men aged 51 to 60, such that higher cortisol output was linked to poorer cognitive performance. In a 35-year longitudinal component of their study, cognitive ability at age 20 predicted midlife salivary cortisol levels, suggesting that factors early in life significantly impact aging outcomes, which vary among individuals. In evaluating this, Franz et al. (2011) cite the vulnerability hypothesis, which posits that cortisol levels and cognitive effects observed late in life originate from pre-existing likely genetically-mediated risk factors.

Our results suggest marmosets do not exhibit senescence of the HPA axis. If this is supported with additional longitudinal and cross-sectional investigation, this opens new areas of investigation to understand the mechanisms of HPA axis maintenance during aging aside from dysregulation. Furthermore, primates such as the common marmoset are important models for identifying factors predictive of individual lifelong glucocorticoid trajectories. Longitudinal investigations into age-related changes in cortisol, obtained both from hair and urinary samples, are essential for understanding these relationships.

Highlights.

  • We quantified hair cortisol concentration over the lifespan in marmosets

  • Infants displayed higher cortisol than all other age groups

  • Marmosets did not exhibit senescence of the HPA axis

  • HPA axis dysregulation may not be an inevitable consequence of aging

Acknowledgements

We are grateful to the veterinary and technical staff at SNPRC for their support of the marmoset colony and for assistance in acquiring hair samples.

Funding

This investigation used resources that were supported by the Southwest National Primate Research Center grant P51 OD011133 from the Office of Research Infrastructure Programs, National Institutes of Health. Additional support was provided by the National Institute on Aging grant R01 AG064091 to KAP and the Neuroscience Program at Trinity University. This content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Abbreviations:

HCC

Hair cortisol concentration

HPA

Hypothalamic-pituitary-adrenal

CV

coefficient of variation

Footnotes

Conflict of Interest Statement

The authors declare no conflicts of interest.

CRediT author statement

Matthew Lopez: Conceptualization, Investigation, Formal Analysis, Writing - Original Draft. Amaya Seidl: Investigation, Writing - Original Draft. Kimberley Phillips: Conceptualization, Investigation, Writing - Review and Editing, Funding Acquisition.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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