Hair cortisol reflects socio-economic factors and hair zinc in preschoolers
Introduction
Childhood experiences may have a life-long influence on the function of the hypothalamic–pituitary–adrenal (HPA) axis and thus on the regulation of cortisol. In children, differences in cortisol levels have been reported in relation to mother's depressive symptoms (Lupien et al., 2001, Essex et al., 2002), childhood adversity (Carlson and Earls, 1997, Gunnar et al., 2001), and stressful neonatal (Grunau et al., 2007) and childhood (Flinn and England, 1997, Gunnar and Vazquez, 2001) environments. Moreover, socioeconomic status (SES) in childhood has been shown to influence cortisol secretion patterns (Lupien et al., 2000, Lupien et al., 2005, Li et al., 2007). Both direct and indirect effects of factors such as pre- or post-natal nutrition, stress, early life adversity, maternal depression and/or environmental (school, home, neighbourhood) variables on HPA development could mediate the association between childhood SES and cortisol. Several studies have shown that cortisol levels are also associated with adult SES (Brandtstädter et al., 1991, Steptoe et al., 2003, Kristenson et al., 2004, Kunz-Ebrecht et al., 2004, Cohen et al., 2006a, Cohen et al., 2006b) and, in fact, gradients in cortisol levels have been shown according to income, education, and occupational status in adult life (Kunz-Ebrecht et al., 2004, Cohen et al., 2006b). Interestingly, one life course study suggested that associations between cortisol secretion patterns and SES in adulthood can be attributed, at least in part, to SES gradients in cortisol in childhood (Li et al., 2007).
Overall cortisol levels or secretion patterns in childhood are important because they are related to trajectories of physical, cognitive and socio-emotional development. Although the direction of association may vary, it has been demonstrated that growth and adiposity trajectories from age 7 to 45 years are associated with cortisol secretion patterns (Power et al., 2006). Moreover, associations between cortisol and childhood cognition have been observed in several studies including the 1958 British Birth Cohort (Power et al., 2008) and in a cross-sectional sample of 53 Spanish children aged 9–12 years (Maldonado et al., 2008), reflecting the fact that the brain is a major target for the glucocorticoid hormones. Importantly, the relationship is bidirectional, with effects of cortisol on cognitive function and, conversely, effects of cognitive processing on cortisol secretion (Lupien et al., 2002, Lupien et al., 2005). The HPA axis is also thought to play a role in socio-emotional development and psychological state (Goodyer et al., 2001, Herbert et al., 2006). Associations between emotional state and cortisol have been observed in infancy (Gunnar and Nelson, 1994, van Bakel and Riksen-Walraven, 2004, Lewis and Ramsay, 2005) and childhood (McBurnett et al., 2000, Shirtcliff et al., 2005, Herbert et al., 2006, Brummelte et al., 2010). One longitudinal study found that preschoolers exposed to high levels of maternal stress had elevated cortisol levels and, in turn, exhibited greater mental health symptoms in first grade (Essex et al., 2002). Over the life course, the HPA axis may become dysregulated due to social stressors (Power et al., 2010), as suggested by studies of low SES and of maltreatment in childhood (Carlson and Earls, 1997, Lupien et al., 2000, Cicchetti and Rogosch, 2001, Gunnar et al., 2001, Gunnar and Vazquez, 2001, Ranjit et al., 2005, O’Connor et al., 2009). In turn, dysregulation of the HPA axis may lead to either hypo- or hyper-secretion of cortisol, carrying increased risk of depression and other mental health problems (Bremmer et al., 2007).
Taken together, this research on the determinants of HPA axis function, cortisol secretion patterns, and life course health and development has generated a tantalizing glimpse of the ‘life’ of a key stress response pathway in human society. However, our understanding of the significance of the HPA axis for human health and development has been hindered to some extent because of limitations in the available methods of cortisol measurement. Accordingly, a principal challenge for studies that seek to understand the relationships among HPA axis function, social factors, life course and health is the method of estimation of cortisol secretion patterns. Cortisol levels in biological samples such as plasma and especially, saliva, have commonly been used as markers of daily HPA axis function and, also, of the HPA response to experimental stressors. However, in the life course context, even multi-time-point, multi-day sampling of saliva or plasma cannot provide a full picture of long-term HPA axis function and cortisol secretion.
In recent years, methods to assay cortisol in hair have been developed that provide an integrated index of cumulative cortisol exposure over an extended period of time. Raul et al. (2004), in the context of tracking illegal use of performance-enhancing steroids by athletes, demonstrated that physiological concentrations of cortisol and cortisone could be detected in human hair. Further studies demonstrated that hair cortisol levels correlate significantly with cortisol in a 24-hr urine sample (Sauvé et al., 2007) and with contemporaneously collected salivary cortisol (D’Anna-Hernandez et al., 2011). Moreover, hair cortisol was shown to correlate positively with waist-to-hip ratio, suggesting that hair cortisol reflects cortisol exposure over the long term at tissue levels (Manenschijn et al., 2011). Subsequent data have supported the use of hair cortisol as an integrated measure of long-term HPA activity. To cite just a few examples, adults with severe chronic non-malignant pain syndromes were found to have increased subjectively perceived stress, as measured by the Perceived Stress Scale questionnaire, and concomitantly, had elevated hair cortisol levels compared to control subjects, suggesting that hair cortisol levels could be a novel biomarker for long-term stress exposure (Van Uum et al., 2008). Steudte et al. (2011) showed that hair cortisol levels were significantly higher in traumatized (from a civil war area of Northern Uganda) individuals with post-traumatic stress disorder (PTSD) than in traumatized individuals without PTSD, suggesting that PTSD in traumatized individuals who continue to live under stressful conditions might reflect general hypercortisolism. Yamada et al. (2007) showed that whereas hair cortisol levels did not distinguish between preterm and term neonates in neonatal intensive care units, they did correlate with number of days on a ventilator in the term born infants, and thus might be a marker of chronic neonatal stress. Hair cortisol levels were also shown to be a useful marker of hypercortisolism in alcohol-dependent individuals (Stalder et al., 2010). Three- to four-fold higher cortisol levels were seen in hair samples from alcoholics during acute withdrawal than in those of abstinent alcoholics or controls. These findings paralleled those of previous work using well-established measures of systemic cortisol secretion. Thus, in a variety of settings, and in both adults and infants, hair cortisol appears to provide an ideal measure to monitor cumulative cortisol release over an extended period of time; providing an integrated measure of exposure to stress and, also, to longer-term HPA axis function. Moreover, hair requires no special handling or storage. Therefore hair provides an ideal tissue for large-scale surveys of prolonged stress levels.
In the literature, stress is also commonly associated with socioeconomic status background. Studies have repeatedly found a correlation between SES (income, education, occupational status) and developmental health outcomes, and researchers therefore speak of the ‘SES gradient of developmental health’ (Keating and Hertzman, 1999). Multiple studies have described the underlying causal mechanisms that associate low SES – poverty in particular – with poor developmental outcomes (e.g., Berliner, 2005). In the context of this study, it is important to note that income and education have been found to be correlated with stress-preventing or -buffering family mechanisms and parenting processes, such as social support, warmth/caring combined with appropriate control/supervision, providing healthy nutrition and regular routines, family violence, unclear and/or age-inappropriate expectations (Dornbusch et al., 1987). These family mechanisms and parenting processes, in turn, are known to have direct impact on the developmental health and well-being of children (Baumrind, 1966, Bronfenbrenner, 2005, Luthar, 2006). Parental education and income may therefore be considered indicator variables of environmental stressors, as they gauge the availability of resources in a family context (e.g., time, money, access to information), and some of these resources represent necessary, though not sufficient, prerequisites for a number of positive family mechanisms and parenting practices (e.g., time to be with children, money to provide safe housing and healthy nutrition and activities, knowledge about child development/parenting).
The aim of the present study was to examine whether in young children, hair cortisol, as an integrated measure of cortisol exposure across an extended period of time is associated with parental SES. Hair cortisol was assessed in relation to gender, parental income and education, family structure, ethnicity, and socioeconomic characteristics of the neighbourhood of residence. Our previous community-based survey of hair zinc, conducted among 342 children age 4–6 years in an ethnically and socioeconomically diverse urban environment (Vaghri et al., 2008, Vaghri et al., 2010), demonstrated an association between maternal education and hair zinc. Hair zinc is considered a biological marker of long-term adequate zinc nutrition; that is, children who have an inadequate zinc intake have lower hair zinc levels than children who have adequate zinc intake (Prasad, 1988). Given the relationship between nutrition and SES (Sandstead, 1973), hair zinc provided an index of adequacy of zinc nutrition to complement the environmental factors described above and to explore the possible relationships between hair zinc and hair cortisol.
Section snippets
Sample
The final sample consisted of 339 children (49% boys; 51% girls; mean age = 4.6 years, SD = 0.5 years) who were recruited from child care centres located in the city of Vancouver, British Columbia, Canada. Below, we provide details on recruitment, inclusion, and exclusion criteria.
In Section 3, we present descriptive statistics for the full sample. For the multivariate analyses, we only included cases with complete data on all variables (n = 273 for the analysis for maternal education; n = 269 for the
Results
Table 1 shows the descriptive characteristics for the child-level factors age, gender, single parent status, maternal and paternal education, ethnicity, family income and hair zinc in relation to hair cortisol. Given its subsequent importance in the analysis, we additionally illustrate the relationship between the four categories of maternal education and the absolute cortisol values in Fig. 1 (as bar graph, mean ± standard error of the mean [SEM]). We note that the relationship between paternal
Discussion
This study is the first to examine hair cortisol, as an integrated index of stress over an extended period of time, and its relationship to social determinants in a community sample of young children. The results indicate that parental education – as indicated by maternal or paternal education – and hair zinc both have significant inverse associations with hair cortisol. These relationships remained significant even after controlling for covariates, such as the child's age, gender, ethnicity,
Endnote
Endnote: As described in the text, the correlation between maternal education and the winsorized and log-transformed cortisol values is statistically significant. In the graph, we illustrate the group means for each for the four groups of maternal education, using the means of the (not-winsorized, not-log-transformed) cortisol values. We note that due to the small cell sizes of the ‘less than high school’ and ‘high school’ groups, a Bonferroni post hoc ANOVA analysis does not show statistical
Role of the funding source
Research was supported by a grant from the Human Early Learning Partnership (HELP), The University of British Columbia, Vancouver, Canada.
Conflicts of interest
All the authors report no potential conflicts of interest.
Dr. Weinberg's research is currently funded by grants from NIH/NIAAA, the Coast Capital Savings Depression Research Fund, and the Canadian Foundation for Fetal Alcohol Research. She receives honoraria from NIH for grant reviews. Dr. Grunau's research is currently funded by grants from NIH/NICHD and CIHR. She receives salary support from the Child and Family Research Institute.
Acknowledgement
Supported by a grant from the Human Early Learning Partnership (HELP), The University of British Columbia, Vancouver, Canada. We are grateful to the children who participated in this study.
References (67)
- et al.
Developmental and personality correlates of adrenocortical activity as indexed by salivary cortisol, observations in the age range of 35–65 years
J. Psychosom. Res.
(1991) - et al.
Major depression in late life is associated with both hypo- and hypercortisolemia
Biol. Psychiatry
(2007) - et al.
Hair cortisol levels as a retrospective marker of hypothalamic-pituitary axis activity throughout pregnancy: comparison to salivary cortisol
Physiol. Behav.
(2011) - et al.
Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior
Biol. Psych.
(2002) - et al.
Seasonal variations in hair zinc concentrations in Canadian and African children
Sci. Total Environ.
(1989) - et al.
Altered basal cortisol levels at 3, 6, 8 and 18 months in infants born extremely low gestational age
J. Pediatr.
(2007) - et al.
Social regulation of the cortisol levels in early human development
Psychoneuroendocrinology
(2002) - et al.
Psychobiological mechanisms of socioeconomic differences in health
Soc. Sci. Med.
(2004) - et al.
Work stress, socioeconomic status and neuroendocrine activation over the working day
Soc. Sci. Med.
(2004) - et al.
Life-time socioeconomic position and cortisol patterns in mid-life
Psychoneuroendocrinology
(2007)
Child's stress hormone levels correlate with mother's socioeconomic status and depressive state
Biol. Psychiatry
The modulatory effects of corticosteroids on cognition: studies in young human populations
Psychoneuroendocrinology
Stress hormones and human memory function across the lifespan
Psychoneuroendocrinology
Cortisol awakening rise in middle-aged women in relation to psychological stress
Psychoneuroendocrinology
Cognitive development and cortisol patterns in mid-life: findings from a British birth cohort
Psychoneuroendocrinology
Detection of physiological concentrations of cortisol and cortisone in human hair
Clin. Biochem.
Zinc nutrition in the United States
Am. J. Clin. Nutr.
Increased cortisol concentrations in hair of severely traumatized Ugandan individuals with PTSD
Psychoneuroendocrinology
Effects of authoritative parental control on child behavior
Child Dev.
Cortisol levels in relation to maternal interaction and child internalizing behavior in preterm and full term children at 18 months corrected age
Dev. Psychobiol.
Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania
Ann. N.Y. Acad. Sci.
Maternal Education, Home Environments and the Development of Children and Adolescents
The impact of child maltreatment and psychopathology on neuroendocrine functioning
Dev. Psychopathol.
Socioeconomic status is associated with stress hormones
Psychosom. Med.
Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study
Psychosom. Med.
The influence of parent education and family income on child achievement: the indirect role of parental expectations and the home environment
J. Fam. Psychol.
Andrew Jackson's exposure to mercury and lead: poisoned president?
JAMA
The relation of parenting style to adolescent school performance
Child Dev.
The family environment in nonorganic failure to thrive: a controlled study
J. Pediatr. Psychol.
Social economics of childhood glucocorticoid stress response and health
Am. J. Phys. Anthropol.
Possible role of cortisol and dehydroepiandrosterone in human development and psychopathology
Br. J. Psychiatry
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