The results of the present study confirmed that even in family-based daycare settings, cortisol levels rise over the day. We also found that certain dimensions of care quality and child behavior were associated with the cortisol rise. Finally, although boys and girls did not differ in their cortisol responses to child care, the associations between child behavior, care quality, and the cortisol rise were moderated by child sex. Thus child sex appears to be a critical factor in understanding the psychosocial processes underlying cortisol stress reactions at child care. Each of these aspects of the results will be discussed below.
The majority of the children showed an increase in cortisol from mid-morning to mid-afternoon at daycare, while at-home levels remained relatively flat over the mid-section of the day. There was no evidence of a sex difference; boys and girls exhibited similar increases in cortisol over the child care day. Furthermore, the lack of a change from morning to afternoon in the home data was the typical diurnal basal pattern for children of this age (Watamura et al., 2004
). Specifically, the basal decline from mid-morning to mid-afternoon has been shown to emerge at home as circadian sleep patterns become more adult-like (i.e., as the child gives up the afternoon nap). In addition, the rise at daycare was relatively stable across the two days of assessment with over half of the children producing a rise from morning levels on each day of assessment. Because even small changes in cortisol could be statistically but not necessarily biologically
significant, we used criteria previously used in adult studies to identify HPA stress responders. This analysis indicated that only 10% of the children exhibited a stress response in the morning at daycare, while 40% could be classified as stress responders in the afternoon.
Taken together these data suggest that a substantial number of children exhibit a stress response of the HPA system over the day at daycare; further, as evidenced by the day-to-day stability data, this occurs on a regular basis for a number of children. It is telling that this response is seen more clearly in the afternoon than the morning, indicating a rising pattern of cortisol over the day. This suggests that the response is not a reaction to arriving at child care in the morning, but a response that emerges over the accumulation of the day's experiences. This may explain why in half-day, preschool programs, cortisol levels are not elevated over home levels for classes that meet in the morning or for those meeting in the afternoon (Gunnar, Tout, de Haan, Pierce, & Stansbury, 1997
), while these elevations are observed by afternoon in full-day programs. The question, of course, is why
. What is it about spending a full day at child care that produces a stress response of the HPA system by the afternoon in so many young children?
We found no significant associations between any of the structural measures of care quality and the rise in cortisol at daycare. Thus, there was no evidence that provider experience or training predicted this rise, nor was there evidence that the rise was related to the number of children in care or the number of adults in the setting. Our failure to find an association with group size was particularly noteworthy. Not only was no linear association found, but when we examined settings with only one or two children in addition to our target child, increases in cortisol over the day averaged the same as increases in settings with 10 or more children.
Previously we have suggested that the complexity of the demands of managing interactions with large numbers of children might account for cortisol increases over the day among children in center-based care settings (Gunnar & Donzella, 2002
; see also Belsky et al., 2007
, regarding the possible importance of the peer group in daycare effects). This argument was predicated on the following findings. In comparing the cortisol response over the child care day for toddlers and preschoolers in center-based care, we did not observe elevations for children cared for in infant rooms (Watamura, Donzella, Alwin, & Gunnar, 2003
). In infant rooms, activities are typically organized around the infant's schedule, which means that at any given time, only a few infants are awake and when awake, they are likely to be interacting with adults. In toddler rooms, however, the children eat, sleep and play at the same times and thus there is much more peer interaction in these rooms. Furthermore, with development over the toddler period, time spent interacting with peers increases (Hughes & Dunn, 2007
). Second, when we examined changes in cortisol over nap time for preschoolers in center-based care, we noted significant decreases from before to immediately after the nap, even for children who did not appear to sleep over the nap period (Watamura et al., 2002
). Because the nap period at child care is one during which children usually do not
interact with other children, the removal of social interaction demands during this period seemed a reasonable hypothesis for why even those children who did not sleep showed decreases in cortisol over the nap period.
The fact that we observed the same cortisol rise in settings with only two or three children that we found in settings with 10 or more children strongly argues against
the social complexity hypothesis, at least with regard to daycare settings. It still might be that center-based child care rooms with many children and adults evoke more of a cortisol response than those with fewer children (see Legendre, 2003
), given that none of our settings were that large. However, the fact that the rise in cortisol by afternoon was observed in very small settings suggests that social complexity is not the primary factor accounting for the cortisol stress response. This conclusion also is consistent with the fact that the present findings are largely consistent with previous findings for children of this age studied in center-based care. The average number of children per each preschool-aged care room in daycare centers ranges between 13.0 (at 36 months; NICHD ECCRN, 1999
) and 15.4 (at 54 months; NICHD SECCYD, 2008
), while the mean number of children in the family daycare homes we studied was around five. One would have expected, therefore, that if the demands of negotiating complex social environments was the key factor, then many fewer children would have shown a cortisol stress response over the day in family-based daycare than has been observed in studies of center-based care. But that was not the case.
We did obtain evidence that our measures of care provider behavior, sometimes termed process
measure of care quality, were related to the rise in cortisol at daycare. Principal factor analysis yielded evidence of two factors: warm and supportive care and intrusive, over controlling care. Child care studies typically identify one dimension of quality that includes both warmth and control dimensions (e.g., NICHD ECCRN, 2000
). As in many studies of parenting (e.g., Barber, Stolz & Olsen, 2005
), these dimensions were distinct in our data. It may be that the use of family daycare settings that were more home-like produced patterns of provider behavior that were more like those seen in parenting research.
Our results also showed that these two dimensions were differentially related to the rise in cortisol at daycare. Specifically, although warm, supportive care was related to our measures of child behavior, it was not associated with the cortisol rise either for boys or girls (although see discussion of moderation by angry, aggressive behavior for boys, below). In contrast, intrusive, over controlling care was associated with larger rises in cortisol over the daycare day. This was true for both boys and girls as gender did not interact with this effect. It is not clear why intrusive, over controlling care was stress-provoking. It may be that this dimension of care reflected a daycare environment that was structured to provide fewer developmentally-appropriate experiences. Anecdotally, settings scoring high in intrusive, over controlling care were often ones in which the children were transitioned frequently between activities, were permitted relatively little time in free play, and spent long periods in provider-directed structured activities. In the Sims et al. (2006)
study, developmentally-appropriate practices related to transitions and scheduling were facets of quality associated with the rise in cortisol for children in child care centers. It may be that when young children are required to manage a day with many structured activities and transitions, this overtaxes their coping capacities as the day progresses. Notably, however, although intrusive, over controlling care accounted for statistically significant variance in the cortisol rise, there was still a good deal of individual variation that was not explained by this process dimension of quality.
Some of this unexplained variance was associated with child behavior patterns at daycare. As expected, two dimensions of behavior were identified. The first dimension involved variation in anxiety and vigilance and in social integration. Children scoring high on this dimension were more anxious and vigilant and were less socially integrated in the setting. The second dimension involved variation in angry mood and negative interactions with peers. Both anxious vigilance and angry, aggressive behavior were observed more in boys than girls. Given the association with the cortisol rise, this would suggest that boys might have experienced more stress at child care than girls. However, as noted above, we found no gender difference in cortisol at daycare. Rather, we found that gender moderated the associations of behavior and rise in cortisol over the day. For boys, larger cortisol increases were associated with more angry, aggressive behavior, while for girls it was associated with more anxious, vigilant behavior.
Other studies of child care have also noted gender differences in associations between child behavioral dispositions and HPA activity. For example, Dettling and colleagues (1999)
found that parent-reported surgency positively predicted the cortisol rise for boys but not girls, while parent-reported effortful control negatively predicted the rise for girls. Why associations might differ for boys and girls is unclear. By adulthood, there are clear differences in reactivity of the HPA axis to stressors, as well as evidence that the type of stressors that most strongly affect men differ from those that are most provocative for women (for review, see Dedovic, Wadiwalla, Engert, & Pruessner, 2009
). For both men and women, threats to the social self stimulate the HPA axis, but for women the most salient threats to the social self appear to be ones that threaten relationships, while for men they appear to be ones that threaten social status and agency (see also Stroud, Salovey, & Epel, 2002
While these gender differences in stress provocation appear to emerge most clearly after childhood (see Stroud et al., in press
), the present results are consistent with the adult findings. That is, larger cortisol increases were observed for the girls who, in addition to being anxious and vigilant, were also less socially integrated into the daycare setting. Our scoring of positive social integration was based on whether the child was central to the action, such that if the child left the activity or decided to change the activity then the other children would follow or play would stop. When combined with anxious, vigilant behavior, our summary score may have reflected anxiety over threats to goals of having and maintaining relationships with peers. If by this young age social relationships are beginning to emerge as a more central goal for girls than boys, then this might explain its greater association with the cortisol rise for girls at daycare. Note that this argument is consistent with evidence that by preschool age, girls use somewhat more relational aggression or actions which threaten relationships than do boys (Crick et al., 1997
This argument does not explain why we obtained a significant association between angry, aggressive behavior and the rise in cortisol for boys but not girls. As noted, our finding for boys was consistent with the meta-analysis of aggressive, under-controlled behavior which provided evidence that while such behavior is associated with low cortisol for school-aged children, among preschool-aged children it is associated with higher cortisol levels (Alink et al., 2008
). What was noteworthy was the gender difference in the association of care quality with angry, aggressive behavior. For both sexes, this behavior was observed more when children were receiving less warm and supportive care, but only for boys was angry, aggressive behavior associated with higher levels of intrusive, over controlling care. In fact, as suggested in , it was at high levels of intrusive, over controlling care that the gender differences in angry, aggressive behavior were most pronounced. This suggests that not only the frequency but the social meaning and function of angry, aggressive behavior may have differed for boys and girls. For boys it may have been a reflection of salient threats to agency, which, even at this age, may be a more central goal for boys than girls. Indeed, this would be consistent with evidence that as early as one year of age, loss of control (agency) over a loud, noise-making toy elicits more negative affectivity in boys than girls (e.g., Gunnar, 1980
), as well as evidence of gendered differences in adulthood in the role of fighting and asserting dominance or control versus seeking relationships in coping with threatening situations (Taylor et al., 2000
The data for angry, aggressive behavior and stress for boys, however, was even more nuanced than gendered association with intrusive, over controlling care would suggest. Specifically, in the moderation analyses we found that among boys, angry and aggressive behavior moderated the association between warm, supportive care and the cortisol rise. Specifically, we found that it was the boys who scored low on this measure whose cortisol rise at child care was associated with the degree of warm and supportive care they received. Under conditions of low warmth and support they showed large increases in cortisol over the day, while under conditions of high warmth they show small increases that were well within the norm for cortisol changes over the day at home. Boys scoring high on angry, aggressive behavior did not show any modulation of the cortisol response to child care in relation to care provider warmth and support. This moderation effect was the opposite of that predicted based on arguments that children who are more vulnerable to behavior problems (e.g., externalizing-type problems in this case) might be more sensitive to variations in care quality. However, as boys were more aggressive than girls, it may be that boys scoring low on angry, aggressive behavior may have had more difficulty managing play with other boys and thus may have been more dependent on the degree of warm, supportive care they were receiving from the care provider.
We recognize that our explanations for the gender differences in cortisol-behavior associations are speculative and that these findings will contribute to continued uncertainty about how behavior in peer settings is associated with activity of the HPA axis in young children. However, they should also encourage researchers to consider the role of gender differences in future studies of child care stress. Our findings suggest that even when boys and girls do not differ in their physiological stress reactions to complex social situations, they may differ in how emotional-behavioral dispositions and patterns of action relate to their stress responses in those contexts. Furthermore, it seems likely given our pattern of results that these gender differences reflect the gendered aspects of children's social worlds and socialization experiences. As noted above, by adulthood there is good evidence for gender differences in stress reactivity and regulation (Dedovic et al., 2009
; Taylor et al., 2000
); thus, an increased focus on gendered patterns of stress-behavior-context associations during development is needed.
One of the challenges of interpreting the present findings is that the associations we found accounted for only modest amounts of the variance in the cortisol rise. For example, our measure of intrusive, over controlling behavior only accounted for 4% of the variance in the cortisol rise, while in combination the child behaviors and their interaction with sex explained 10% of the variance. It is likely that our methods limited the amount of variance that we could explain. First, cortisol and behavior were measured on different days, and there was likely error in our measures such that behavior on one the days of observation was not exactly the behaviors we would have observed had we measured on the days of cortisol assessment. Unfortunately, the M-ORCE, like the ORCE, requires summating over the two days of observation, thus we do not have a measure of day-to-day variability in either our two process measures of quality or our two measures of child behavior. For the cortisol rise, although we observed a significant correlation across the two days of assessment, the rise on day one explained only 16% of the variance in the rise on day 2. Thus, limitations in the method likely limited the magnitude of the associations we could hope to find. Nonetheless, the effect sizes we observed were consistent with others often reported in child care studies, and it has been argued that such effect sizes should not be dismissed in considering the import of findings for child care policy and practice (McCartney & Rosenthal, 2000
Our findings provide added impetus to the effort to understand whether and how HPA stress responses at child care impact children's development. Although early life stress is typically viewed as a risk factor for healthy development, recent studies in both non-human primates and in human populations raise questions about this type of blanket assessment of early life stressors. For example, Lyons and Parker (2007)
have examined the impact of repeated, one-hour separations in infant squirrel monkeys. As in the work on cortisol responses to full-day child care, these separations in squirrel monkey infants produced marked and repeated activations of the HPA axis. However, followed into the late juvenile and early adult age, animals exposed to this form of early life stress were found to be less fearful, to produce lower rather than higher cortisol responses to stressors, and to show more optimal development of prefrontal regulatory brain circuits; consistent with these findings, they also performed better on tests of executive functioning. Thus, at least for this animal model, repeated separation stress early in life fostered a form of resilience.
In studies of human populations, most of the work on early maltreatment and risky family patterns has been conducted on adults with various affective disorders. Here the evidence is that early life stress produces hyper-reactivity of the HPA axis, consistent with views that early life stress enhances the neural substrate underlying vulnerability to affective disorders (e.g., Heim, Plotsky, & Nemeroff, 2004
). However, in recent studies, researchers have sought to examine the associations between early life stressors and HPA reactivity among adults who are free of significant internalizing pathology. These studies are showing hypo-activity of the HPA axis compared to healthy adults without early life stressors (Carpenter et al., 2007
; Elzinga et al., 2008
). These findings are also consistent with recently reported evidence that teenagers who experienced more full-time, center-based daycare under the age of three produce lower than average levels of cortisol early in the morning at the peak of the diurnal cycle (Roisman et al., in press
). We clearly need to continue to be cautious about interpreting the implications of cortisol elevations in daycare. Nonetheless, evidence that this rise is associated with anxious, vigilance (i.e., internalizing) behavior for girls and anger, aggression (i.e., externalizing) behavior for boys should not make us sanguine about its potential implications for children's development.
Several limitations in this study also should be noted. First, although we included family demographic factors in our analyses, we did not examine the quality of parent-child relations and their associations with the daycare cortisol rise. As in other studies of child care effects, it is possible that issues in the children's families carry more of the weight in predicting how the child responds to child care than issues within the child care setting (Ahnert & Lamb, 2003
; Phillips et al., 2006
; Love et al., 2003
). Although we did not attempt to pre-select for parents with fairly high educations, incomes, and marital status, the variation in family characteristics was quite narrow, reflecting fairly advantaged and low-risk segments of the U.S. population. It may well be the case, as has been found in prior research (Loeb, Fuller, Kagan, & Carrol, 2004
; NICHD ECCRN, 2001
), that quality of child care matters more for low-income children and may thus play a stronger role as an influence on cortisol elevations for children from disadvantaged backgrounds. We were not able to randomly assign children to daycare homes, and thus selection factors could not be controlled in our analyses. We only included licensed daycare homes in our analyses, and thus cannot generalize to effects in the many unlicensed settings used for daycare. Finally, although we worked to increase our racial-ethnic variation, the sample was still predominantly white and of European heritage. This again limits generalizability.
With these limitations, however, we have clearly documented that, similar to children in center-based care, many children in family daycare settings show a substantial rise in cortisol over the day, and they do not show this rise when at home. We have found that this rise is observed even in care settings with only two or three children, thus arguing against the hypothesis that social complexity is a major factor underlying increasing activation of the HPA stress response. We also noted associations between intrusive, over controlling care and the rise in cortisol for both boys and girls and between warm, supportive care and the cortisol rise for less angry, aggressive boys. These findings may help refine our attempts to understand aspects of child care that promote increases in cortisol in young children. Finally, the gendered differences in associations we noted should focus attention on understanding how boys and girls may differentially process and experience stressors in child care settings.