Poverty-alleviation program participation and salivary cortisol in very low-income children
Introduction
The effects of growing up in poverty extend from infancy through adolescence and into adulthood (Bradley & Corwyn, 2002) and include poor health, cognitive and socioemotional delays and behavioral problems (Evans, 2004). For most child health outcomes, there is a gradient in which lower family socioeconomic status (SES) and material well-being is associated with concurrently poorer outcomes (Chen & Matthews, 2006). Experiencing poverty during childhood also appears to have an independent effect on later health outcomes including decreased life span and increased morbidity, even while controlling for adult SES or social status (Poulton et al., 2002). Children growing up in poverty, whether indexed by the family's income or, in low technology cultures, by other indices of the family's material well-being are exposed to a wide range of risk factors, and these conditions are exacerbated in the developing world (Walker et al., 2007). An estimated 219 million children (39% of all children in developing countries) have evidence of signs of poor development at multiple levels (Grantham-McGregor et al., 2007).
The multiple mechanisms through which poverty produces poor outcomes are being actively explored. Lack of income leading to deficiencies in material well-being (e.g., inadequate housing, medical care, food, clothing) is associated with greater exposure to stressors (Elder, 1985). These stressors, ranging from increased exposure to pathogens to increased exposure to violence, activate the hypothalamic–pituitary–adrenocortical (HPA) system. The HPA system is one of the primary components of the mammalian stress response system (Gunnar & Davis, 2003), and is one mechanistic pathway that has received significant theoretical attention (McEwen & Seeman, 1999). When the brain first perceives a stressor, neural input to the hypothalamus induces secretion of corticotropin-releasing hormone (CRH), which stimulates release of adrenocorticotropic hormone (ACTH) from the pituitary gland followed by the release of cortisol from the cortices of the adrenal glands. Following exposure to a stressor, it typically takes 20–30 min for cortisol levels to reach their peaks (De Kloet, 1991); multiple negative feedback mechanisms inhibit further production of CRH and ACTH (Gunnar, Bruce, & Hickman, 2001). Cortisol rises in situations associated with physical and psychological stressors, including inflammatory immune responses, heat or cold stress, novelty or uncertainty, social conflict, negative emotions and feelings of threat or loss of control (Kirschbaum & Hellhammer, 1994).
In the developed world, higher SES children have lower cortisol concentrations than lower SES children (Essex, Klein, Cho, & Kalin, 2002; Evans and English, 2002, Evans and Kim, 2007; Lupien et al., 2000, Lupien et al., 2001). These associations have been confirmed in some, but not all, studies in adults (Cohen et al., 2006, Dowd and Goldman, 2006). To our knowledge, only two studies have examined economic background and how it relates to stress response in children in a developing country. One study (Flinn and England, 1997, Flinn and England, 2003) examined generally low SES children in Dominica. Within the range of economic circumstances they examined, there was no evidence that material benefits (improved housing or diet) were associated with salivary cortisol levels. They did find, though, that children from unstable family backgrounds had higher cortisol levels than did children from stable family homes. The other study set in Nepal measured morning cortisol and a composite index of physiologic functioning, allostatic load, created using cortisol and cardiovascular variables. The physiologic measures differed according to context in which a child lived (e.g., homeless, squatter, village or school) (Worthman & Panter-Brick, 2008); boys who were in school showed a healthier stress profile than those who were squatters or those who were homeless.
Thus, in spite of the small handful of studies that have shown that lower SES is linked with higher and/or dysregulated cortisol, there remains a large research gap relating to whether and how poverty and cortisol are related in young children. Most critically, none of the studies that have examined socioeconomic status and activity of the HPA axis in children or, for that matter, in adults have randomly assigned participants to their economic conditions. Normally, this scenario would not be possible and we would be left with correlational findings where the direction of effects and the potential mediators of the associations could not be wholly examined. Thus, the primary goal of this study was to examine the association between income and children's cortisol levels using participants drawn from a large-scale, randomized poverty-alleviation intervention. This sample allowed examination of the causal relation between income and children's cortisol levels. In addition, because few of the studies of SES and cortisol have examined children living in extreme poverty, the present study extends existing research on poverty and children's HPA axis activity to children experiencing the type of extreme poverty that is prevalent in many developing countries.
The studies cited above that have found that lower SES is associated with higher cortisol levels in children have all also reported that the effects of lower SES may be mediated, at least in part, by maternal depressive symptoms (Bradley & Corwyn, 2002). Maternal depression is associated with having lower income and greater income insecurity in both the developed and developing world (Hadley and Patil, 2008, Pascoe et al., 2006). When parental care is poor or frequently disrupted during early development, increased levels of cortisol are released in response to threat as measured later in life (Meaney & Szyf, 2005). Depressed mothers tend to provide less sensitive and responsive care to their infants and young children, particularly in the first year of life (Dawson & Ashman, 2000). Further, children of depressed mothers are often less able to meet their children's age-appropriate and stage-salient needs (Arcenio, Sesin, & Siegel, 2004).
If maternal depression serves to influence the impact of SES on children's cortisol levels, then within the context of a poverty-alleviation intervention study, this would argue for examination of maternal depression as a moderator variable. That is, if under the no-treatment condition children of mothers with high depressive symptoms show the most dysregulated pattern of cortisol production, then under the treatment condition, children of depressed mothers may show the greatest impact on HPA activity. There are also other reasons that maternal depression might moderate child HPA axis activity (Goodman & Gotlib, 1999). Depressed mothers may pass genes to their children that increase the reactivity of the axis to the conditions (pathogens, food insecurity) associated with poverty (Goodman, 2003). Similarly, they may expose their infants to elevated stress hormones during prenatal development, and these exposures may increase the sensitivity of the HPA system to postnatal conditions. Thus, using a construct introduced by Boyce and Ellis (2005), the offspring of depressed mothers may be more sensitive to context, showing larger differences than the offspring of non-depressed mothers in response to better or worse family-level factors.
However, there is also a substantial animal and human literature indicating that when parental care is actively supportive, offspring can be relatively buffered from the impact of a variety of stressful events (see review, see Gunnar & Donzella, 2002). This process – maternal or parental buffering – reflects the capacity of a supportive adult to prevent or reduce elevations in cortisol, perhaps through stimulation of “anti-stress” hormones such as oxytocin (e.g., Carter, 1998). A responsive and high-functioning mother, however, may also regulate stress experiences in her offspring through active management of the environment (Leiferman, 2002, McLennan and Kotelchuck, 2000).
Previously, among 2.5- to 6-year old children growing up in urban poverty in Mexico, we reported that among offspring of depressed relative to non-depressed mothers, maternal depression did not affect baseline cortisol levels, but did affect salivary cortisol response to the same mild stressor used in this report (Fernald, Burke, & Gunnar, 2008). Unexpectedly, rather than maternal depression being associated with increased cortisol reactivity, it was associated with a blunted cortisol response. While the blunted response was unanticipated, it may have reflected the impact of chronic stress down-regulating activity of this system (see Miller, Chen, & Zhou, 2007). Thus, there are both theoretical and empirical data suggesting that maternal depression might amplify the effects of poverty on the developing HPA axis.
The present study uniquely contributes to the literature by using a planned quasi-experimental design to test the impact of Oportunidades – a large-scale, poverty-alleviation program – on salivary cortisol concentrations in 2- to 6-year-old children in rural areas. The goals of the study were to provide an empirical test of the association between the economic conditions of early life rearing and child cortisol levels through examining the impact of family-level participation in Oportunidades. Based on previous evidence of a negative association between SES and children's cortisol levels, we hypothesized that children whose families participated in the program would have lower baseline cortisol levels and clearer evidence of a modulated (i.e. rise and return to baseline) cortisol response to the psychosocial stressor task. The less modulated response might include either failure to return to baseline within the sampling period and/or failure to mount a significant response to the stressor tasks. Both patterns of hyper- and hypo-responsiveness of the HPA axis have been observed in response to chronic stress (Fries et al., 2005, Heim et al., 2000).
A second objective was to examine whether maternal depression moderated the response to program participation. This objective was supported by previous research showing that child's cortisol responses are influenced by parental stress (e.g., due to marital conflict) (Flinn, 2006) and maternal depression (Ashman et al., 2002, Essex et al., 2002, Lupien et al., 2000). During the first years of life, a child's relationship with his or her primary caregiver serves as a significant regulator of reactivity of the HPA axis (Gunnar & Donzella, 2002) and we expected that disturbances in this association due to high maternal depressive symptoms might moderate the impact of the poverty-alleviation program on children's cortisol levels.
We chose preschool-aged children for this analysis because alterations in activity of the HPA axis from birth through the early years of life have been hypothesized to affect rapidly developing neural systems involved in emotion- and behavior-regulation (Sullivan & Gratton, 2002).
Section snippets
Intervention
Oportunidades – a large-scale conditional cash transfer program – began in 1997 and was designed to relieve extreme poverty in Mexico; it has been used as a model for initiatives throughout the world. Unrestricted cash payments – typically worth about 20–30% of household income – were distributed by the program only if children, pregnant women, lactating women, and other family members complied with a series of requirements, including prenatal care, well baby care and immunization, nutrition
Sample characteristics
A total of 1197 children aged 2–6 years from rural areas of Mexico participated in the study. The mean age of the sample was 49.0 (SD = 13.9) months. Characteristics of intervention and comparison households are presented in Table 1. The groups were well matched according age, gender and time since wake-up of the participants. Other characteristics were similar including maternal depressive symptoms, the proportion of the sample that had received some primary education, and the index of
Discussion
Previous studies have yielded evidence that socioeconomic status is negatively associated with salivary cortisol levels in children. Nonetheless, while growing up under conditions of poverty has been hypothesized to cause changes in HPA axis activity, this hypothesis has never been tested experimentally. The present study provides the first evidence in support of this causal hypothesis. Children who were born into families who had been assigned to the Oportunidades, poverty-alleviation program,
Acknowledgements
This research was supported by the Oportunidades program, the John D. and Catherine T. MacArthur Foundation Network on SES and Health, the Fogarty International Center of NIH (K01 TW06077, PI Lia Fernald), NICHD (R01 HD40864, PI Paul Gertler) and NIMH (K05 MH66208, PI Megan Gunnar). The authors thank Ryo Shiba, Francisco Papaqui, Gustavo Olaiz, Aurora Franco, Mauricio Hernandez, Stefano Bertozzi, Lynnette Neufeld and Juan Pablo Gutierrez at Mexico's National Institute of Public Health (INSP),
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