Do social disadvantage and early family adversity affect the diurnal cortisol rhythm in infants? The Generation R Study
Introduction
Early life adversity has been associated with a broad range of negative mental health outcomes in adulthood, like post-traumatic stress disorder (Koenen et al., 2007), depression and anxiety (Levitan et al., 2003). Moreover, early adversity can already lead to behavioral problems in childhood that continue through adolescence and adult life (Appleyard et al., 2005). Indeed, there is strong evidence from studies in children that early environmental risk factors increase the risk of behavioral problems, such as symptoms of attention-deficit/hyperactivity and conduct disorder (Counts et al., 2005). Flaherty et al. (2006) also found that early adversity is associated with poor physical health in children.
Early adversity, however, involves a broad range of disadvantages to which a child can be exposed to. Socio-economic disadvantage has been associated, for instance, with developmental delays in 3-year-old children (Emerson et al., 2009) and with poorer child behavioral outcomes in 5-year-olds (Kohen et al., 2008). Likewise, family adversities have consistently been associated with poor childhood outcomes. Maternal depression, poor parenting and parenting stress are major family risk factors for psychosocial problems in the offspring (Petterson and Albers, 2001, Crnic et al., 2005). In addition, other possible risk factors early in life such as maternal smoking during pregnancy and low birth weight are also known to have an impact on behavioral problems in children (Robinson et al., 2009, Alati et al., 2009).
In response to physical or psychosocial stress, the hypothalamic–pituitary–adrenal (HPA) axis, one of the body’s primary stress systems, is activated resulting in short term release of cortisol (Orth and Kovacs, 1998). Chronic exposure to stress early in life may lead to re-adaptations of the HPA axis activity. One of these alterations is dysregulation of the diurnal cortisol rhythm. In healthy adults the normal diurnal rhythm is characterised by post-waking peak cortisol levels (cortisol awakening response) and subsequent declining cortisol levels throughout the day (Edwards et al., 2001). Altered diurnal rhythms have been associated with different kinds of stressors, e.g. work-related stress is related to elevated evening cortisol levels (Rydstedt et al., 2008).
Early childhood adversity has been associated with altered diurnal cortisol rhythms in both adolescence and adulthood. In general, findings indicate that early adversity is associated with higher basal cortisol levels throughout the day or a flatter diurnal slope (Nicolson, 2004, van der Vegt et al., 2009). Furthermore, associations with altered morning cortisol levels have also been found. Both lower morning levels in adults (Meinlschmidt and Heim, 2005) and higher morning levels in adolescents (Halligan et al., 2004) were reported. However, it remains unclear whether these altered diurnal rhythms are a consequence of early adversity, since most studies of childhood adversity were retrospectively reported by adults.
Severe early adversity has also been associated with altered diurnal cortisol rhythms in children. Romanian orphan-reared toddlers exhibited low morning cortisol levels and blunted diurnal cortisol patterns (Carlson and Earls, 1997). In contrast, when Romanian orphans were examined six and a half years after adoption, those adopted after more than 8 months of institutionalization showed higher levels of cortisol across the day (Gunnar et al., 2001). Dozier et al. (2006) found both patterns of low and high cortisol production in foster children aged 20 to 60 months, compared with children who were never in foster care. More recently, Bruce et al. (2009) found that different early adverse experiences can lead to both low and high morning cortisol levels in 3- to 6-year-old foster children. However, these studies in high risk samples cannot be translated easily to the general population.
The inconsistencies of these studies of early adversity in children make interpretation of its influence on the HPA axis activity difficult. Firstly, the HPA axis develops and matures in early childhood. Infants are born without a diurnal cortisol rhythm; this rhythm probably emerges during the first 18 months of life (Gunnar and Donzella, 2002, Herbert et al., 2006). Watamura and colleagues (2004) even posited that the maturation of the HPA axis continues to the third year of life. Moreover, sampling salivary cortisol in infants is difficult (Egliston et al., 2007). Subsequently, only few studies have focused on the influence of early adversity on the diurnal cortisol rhythm in infants and toddlers. Recently, Ouellet-Morin and colleagues (2009) examined the influence of early family adversity on diurnal cortisol activity in 6-month-old twins. They found that early family adversity modulates the heritability of morning cortisol levels in infants. Family adversity was defined by seven risk factors (prenatal maternal smoking, low birth weight, low family income, low maternal education, single parenthood, young motherhood, and maternal hostile behaviors). However, by studying a cumulative index of different family adversity factors, the effect of individual indicators of early family adversity on diurnal cortisol secretion in infants cannot be understood.
The objective of the present study is to study the effects of indicators of social disadvantage and other early adversities on the diurnal cortisol rhythm of infants in a population-based cohort. Studying risk factors occurring early in life in relation to infant cortisol rhythms may help further understand the pathway through which dysregulation of the HPA axis and psychopathology occurs. We hypothesize that infants in the second year of life show a diurnal rhythm of cortisol secretion and that this rhythm, even at a young age, is influenced by several risk indicators of early adversity.
Section snippets
Setting
This study was embedded within the Generation R Focus Study, a cohort study investigating growth, development and health from fetal life onwards in Rotterdam, the Netherlands, which has been described in detail elsewhere (Jaddoe et al., 2008). The Generation R Focus Study, a subgroup within the Generation R Study, was conducted to obtain detailed measurements of the child’s development in an ethnically homogeneous group of indigenous Dutch children to exclude confounding or effect modification
Results
Table 1 shows the characteristics of our study population. Mean maternal age at enrolment was 31.9 years; only one mother (0.3%) was younger than 20 years. Furthermore, only 14 single mothers (3.8%) were present in our sample. 38.5% of the mothers had a high educational level, i.e. university level or higher, indicating higher socio-economic status. Parents sampled the saliva for cortisol of their children between the ages of 11.7 to 19.3 months.
Maternal age was not associated with the AUC (β
Discussion
The present study showed that socio-economic disadvantage and postnatal parenting stress were associated with the diurnal cortisol rhythms of infants aged 12 to 20 months. Low family income showed the clearest relationship with the diurnal cortisol rhythm; infants of low income families showed higher cortisol levels during the day and a more positive cortisol awakening response (CAR), compared with infants of high income families. Also maternal smoking during pregnancy, another indicator of
Acknowledgments
The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the Erasmus University Rotterdam, School of Law and Faculty of Social Sciences, the Municipal Health Service Rotterdam area, Rotterdam, the Rotterdam Homecare Foundation, Rotterdam, and the Stichting Trombosedienst & Artsenlaboratorium Rijnmond (STAR), Rotterdam. We gratefully acknowledge the contribution of general practitioners, hospitals, midwives and pharmacies in Rotterdam. The first phase of the
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