Abstract
Child executive functions (cognitive flexibility, inhibitory control, working memory) are key to success in school. Cortisol, the primary stress hormone, is known to affect cognition; however, there is limited information about how child cortisol levels, parenting factors and child care context relate to executive functions in young children. The aim of this study was to examine relationships between child cortisol, parenting stress, parent coping, and daycare quality in relation to executive functions in children aged 3–5 years. We hypothesized that (1) poorer executive functioning would be related to higher child cortisol and higher parenting stress, and (2) positive daycare quality and positive parent coping style would buffer the effects of child cortisol and parenting stress on executive functions. A total of 101 children (53 girls, 48 boys, mean age 4.24 years ±0.74) with complete data on all measures were included. Three saliva samples to measure cortisol were collected at the child’s daycare/preschool in one morning. Parents completed the Behavior Rating Inventory of Executive Function – Preschool Version (BRIEF-P), Parenting Stress Index (PSI), and Ways of Coping Questionnaire (WCQ). The Early Childhood Environment Rating Scale – Revised (ECERS-R) was used to measure the quality of daycare. It was found that children with poorer executive functioning had higher levels of salivary cortisol, and their parents reported higher parenting stress. However, parent coping style and quality of daycare did not modulate these relationships. Identifying ways to promote child executive functioning is an important direction for improving school readiness.
Keywords: Child stress, Executive function, BRIEF-P, Daycare, Coping, Parenting stress, Cortisol
Executive functions are key to school readiness and academic performance. Development of executive functions has been found to be more related to school readiness than entry-level reading skills, math skills (Blair & Razza, 2007), and intelligence (McClelland, Morrison, & Holmes, 2000), and also predicts a variety of skills involved in academic success in kindergarten and later in childhood (Espy, 2004). Also called cognitive control, executive functions are a highly complex set of processes essential for regulating behavior, planning and problem-solving (Miller & Cohen, 2001). Executive functions are often considered as comprising primarily inhibitory control (resisting distractions), working memory (mentally holding and using information), and cognitive flexibility (adjusting to change) (Diamond, 2006). However, abilities under the umbrella of executive functioning may also include strategic planning, abstract reasoning and decision-making (Alexander & Stuss, 2006; Bechara & Van Der Linden, 2005).
Studies of executive functions in preschool-age children are advancing our understanding of the cognitive abilities that underlie academic success (Espy, 2004). For example, inhibitory control and attention-shifting in preschool are related to a wide range of math and literacy abilities in kindergarten (Blair & Razza, 2007). Further, working memory in preschool children aged 4.5 years was found to predict math achievement in the third year of primary school (3 years later), while executive function skills in the same children in preschool predicted learning in general in grade 3 (Bull, Espy, & Wiebe, 2008). Alternatively, deficits in emotional and/or behavioral executive functioning have been linked to such negative outcomes as aggressive behavior in healthy children (Ellis, Weiss, & Lochman, 2009; Raaijmakers et al., 2008). In school-age children there is considerable evidence that executive functions reflect several subdomains (e.g., Diamond, 2006), whereas in preschoolers executive functions may reflect more general cognitive control (Espy, 2004).
Cortisol, Caregivers and Neuropsychology
Cortisol is the primary biomarker of stress in humans (Gunnar, Bruce, & Hickman, 2001) and high levels of salivary cortisol have been associated with poorer cognitive performance across the lifespan (Lupien et al., 2005; Lupien, Maheu, Tu, Fiocco, & Schramek, 2007). For adults, the impact of stress on cognitive functions is well established. For example, lower performance on tasks of declarative memory and attention are associated with higher cortisol in adults (Elzinga Bernet, Bakker, & Bremner, 2005; McCormick, Lewis, Somley, & Kahan, 2007). Higher stress, as measured with salivary cortisol, has also been demonstrated to impact adult decision-making (Starcke, Wolf, Markowitsch, & Brand, 2008), executive functions (Stawski et al., 2011), and dual-performance activities (Plessow, Schade, Kirschbaum, & Fischer, 2012). Stress and neuropsychology in children has received attention (e.g., Chen, Raine, Soyfer, & Granger, 2015; Hostinar, Johnson, & Gunnar, 2015); however, the literature remains limited.
Children aged 9–12 years with high daily perceived stress had lower morning cortisol levels, and demonstrated significantly poorer scores for speed of memory and continuity of attention (Maldonado et al., 2008). Somewhat consistent with those findings, Quas, Bauer, and Boyce (2004) found a link between cortisol reactivity and short-term memory for children aged 4–6 years . Using parent-reported indicators of executive functions, Miller, Chen, and Zhou (2007) found relationships between markers of regulatory capacity and early school adjustment. Furthermore, Blair, Granger, and Peters Razza (2005) reported that the pattern of cortisol expression was associated with measures of executive functions and self-regulation, confirming the importance of child stress and regulatory capacities.
Parenting stress is known to be a moderator of the relationship between cortisol and attention in infancy (Tu et al., 2007), and it is therefore likely that parenting/ caregiver stress may influence cortisol levels and/or executive functions at preschool age. Brummelte, Grunau, Synnes, Whitfield, and Petrie-Thomas (2011) reported that increased parenting stress over time in toddlers born very preterm may reflect realistic concerns regarding their developmental progress. Geoffroy, Cote, Parent, and Seguin (2006) examined the impact of daycare on cortisol levels for infants, preschoolers, and school-age children across 11 published studies and found that cortisol levels were higher during daycare hours, but that this effect was only evident for children in low-quality care. The effect was also found to be greater for preschoolers and children with difficult temperaments, compared to infants, school-age children, and children with less difficult temperaments. In a published abstract, Alwin (2006) reported few differences between the cortisol levels of children aged 3–18 months when in the home versus a daycare environment and increased cortisol levels in children with distress-prone temperaments and/or of older ages. Also, positive engagement with a caregiver was found to have a buffering effect on cortisol secretion. Moreover, Vermeer and van Ijzendoorn (2006) concluded that cortisol secretion was especially prominent in children attending daycare at less than 36 months of age.
McLuckie (2013) provides a published abstract that describes a strong link between parenting stress and parent-reported child difficulties with emotional control and inhibition. A lesser, but still important, relationship was also found between child initiation and self-monitoring, and parenting stress. In another recent abstract, Cutuli (2012) evaluated the relationship between salivary cortisol, executive functions, living context and parenting behavior. His results suggested no relationship between cortisol levels and high rates of stressful and/or negative life events, or positive parenting behavior. In contrast, in interactive situations, harsh, hostile, or insensitive parenting behaviors were related to increased child cortisol. In addition, initial cortisol levels were found to be negatively associated with executive functions.
Given the previous studies that have shown that child cortisol levels are sensitive to aspects of childcare (e.g., quality of the childcare setting; Geoffroy et al., 2006) and since young children spend many daytime hours in childcare, we thought it important to examine the relationship of cortisol levels during childcare in relation to child executive functions.
Aims of the Current Study
There is a notable lack of research on the relationships between parenting/ caregiver self-reported stress and cortisol, and parenting/caregiver stress and child executive functioning. To our knowledge, Cutuli’s (2012) dissertation abstract is the only available information describing the relationship among these three variables. The aim of the present study was to address these identified gaps in the literature by examining relationships between child cortisol, parenting stress, parent coping, and quality of daycare, in relation to executive functions in children aged 3–5 years. In particular, we were interested in evaluating these relationships using an ecologically valid (report) measure of child executive functions. To our knowledge, all available studies involving child cortisol and executive functions have only been tested with performance-based tasks rather than a parent-reported questionnaire of everyday functioning (Isquith, Gioia, & Espy, 2004). Parent report was chosen in order to reflect typical executive functioning across environments, including those with less structure than that provided during child care hours (e.g., home, community). Using the Behavior Rating Inventory of Executive Function – Preschool Version (BRIEF-P) as a measure of executive functions, we hypothesized that poorer parent ratings of child executive functions would be related to higher child cortisol, higher parenting stress and poorer quality of daycare, and that a positive parental coping style would buffer the effects of child cortisol and parenting stress on executive functions.
METHODS
Participants
Children were recruited from 17 daycares/preschools in three communities in the interior of the province of British Columbia, Canada. A total of 150 parents gave informed consent. Saliva samples were collected from 148 children, since two children did not attend daycare/preschool on the days of saliva sample collection. One child diagnosed with Autism Spectrum Disorder (ASD) was also excluded, as previous literature suggests higher stress levels for parents of children with ASD (e.g., Sharpley, Bitsika, & Efremidis, 1997). Further, salivary cortisol assays were insufficient on one or more samples from eight children. For the questionnaire data, of the 147 respective potential parent participants, 109 parents (74%) returned completed questionnaires. Taking both physiological and questionnaire data together, we achieved complete data (3 assays and completed parent questionnaires) for a total of 101 children (53 girls, 48 boys, mean age 4.24 years ±0.74).
Measures and Procedure
Child Salivary Cortisol
We collected three saliva samples in the mid-to-late morning on one day at the child’s daycare/preschool. The average time of day was 10:42 am for the first sample, 11:02 am for the second sample, and 11:19 am for the third sample, with a mean collection time of 37 min (±11) for all three samples, and an average of 18 min (±6) between the samples. We chose mid-to-late morning to avoid mealtimes and naps, and it appeared to be the most optimal time to reflect the child’s inherent stress level during a time of day important for focused learning. Since salivary cortisol fluctuates, we collected three samples. No child had anything to eat or drink for at least 30 min before the first saliva sample, or during the entire sample collection period. Between samples, children returned to their usual daily activities. Samples were collected in small groups by a research assistant in the presence of at least one daycare staff member. Each child was given a sorbette (Salimetrics®) to place under the tongue for at least 60 seconds. After absorption, the sorbette was placed into an eppendorf tube and kept at 4°C until it was spun to extract saliva. Extracted saliva was then stored frozen at −20°C until assayed. The Salimetrics high sensitivity salivary cortisol enzyme immunoassay kit was used for quantitative determination of salivary cortisol levels. All samples were assayed in duplicates. The intra-assay coefficient of variation was 4.38% and the intra-assay variability was 6.62%, similar to that reported by the kit manufacturer.
Parent Questionnaires
Parents were given three questionnaires at the end of the day on which saliva samples were collected from their children and were asked to complete and return them by mail.
The BRIEF-P (Gioia, Espy, & Isquith, 2003) was developed for children aged 2–5 years and was used to measure executive functions. The BRIEF-P parent response measure is designed to evaluate a child’s executive function capabilities in “real world” settings (Gioia et al., 2003). It contains 63 items that yield five theoretically and empirically derived clinical scales: Inhibit (control of impulses and modulation of behavior), Shift (flexible transition between situations), Emotional Control (modulation of emotional responses), Working Memory (holding of information in mind for completing a task or making the appropriate response), and Plan/Organize (anticipation of future events, use of goals or instructions to guide behavior in context and thinking ahead). These scales yield an overall Global Executive Composite score and three index scores: Inhibitory Self-Control, Flexibility, and Emergent Metacognition, which we used in the present study. The BRIEF-P is sensitive to individual variation in the general population (Isquith et al., 2004) and has been previously used to assess differences in executive functioning in clinical populations of preschool children (Ganesalingam et al., 2011; Mahone & Hoffman, 2007). To our knowledge, the BRIEF-P is the only standardized executive functions questionnaire designed specifically for use with preschoolers. With respect to questionnaire measures such as the BRIEF for school-age children, and the BRIEF-P, concerns have been raised regarding the low to moderate correlations between parent ratings of child executive functions and neuropsychological testing (Anderson, 2001; Anderson, Anderson, Northam, Jacobs, & Mikiewicz, 2002; Denckla, 2002). Despite these findings, the increased ecological validity of parent and teacher reports has been considered an important and non-dismissible contributor to the assessment of executive functions (Gioia & Isquith, 2004; Gioia, Isquith, Guy, & Kenworthy, 2001). Moreover, preschool executive functioning abilities assessed via parent/caregiver report using the BRIEF-P predict early mathematics achievement (Clark, Pritchard, & Woodward, 2010) and the BRIEF parent/teacher forms effectively discriminate children with Attention Deficit Hyperactivity Disorder and other problems (Mahone et al., 2002; McCandless & O’Laughlin, 2007). Therefore, parent and teacher reports are viewed as providing ecologically valid measures of child executive functions. In this study we only used the parent version.
The Parenting Stress Index (PSI; Abidin, 1995) long form was used to examine aspects of stress that stem from the parenting role. The PSI is the most widely used measure of parenting stress in parents of young children with a variety of health, developmental and behavioral problems (e.g., Brummelte et al., 2011; Collett, Cloonan, Speltz, Anderka, & Werler, 2012; Faught, Bierl, Barton, & Kemp, 2007; Fite, Stoppelbein, & Greening, 2008; Glenn, Cunningham, Poole, Reeves, & Weindling, 2009; Tu et al., 2007; Webster, Majnemer, Platt, & Shevell, 2008). The PSI long form contains 120 items comprising three domains: Child Domain, Parent Domain, and Life Stress Domain. The Parent Domain assesses aspects of stress related to the parent’s functioning, and is composed by seven subscales: Competence, Isolation, Attachment, Health, Role Restriction, Depression, and Spouse. The Life Stress Domain provides an index of the amount of stress experienced by the parent outside the parent-child relationship. The Child Domain reflects stress that stems from child characteristics that make it difficult for parents to fulfill their parenting roles. Only the Parent Domain and Life Stress PSI subscales were used for the present study.
The Ways of Coping Questionnaire (WCQ; Folkman & Lazarus, 1988) was used to measure parent coping. The WCQ is a 66-item inventory listing a wide range of thoughts and behaviors used to deal with stressful situations, yielding eight coping scales: Confrontative Coping, Distancing, Self-Controlling, Seeking Social Support, Accepting Responsibility, Escape-Avoidance, Planful Problem Solving, and Positive Reappraisal. The internal consistency coefficients ranged from .68 to .79 for the subscales (Folkman & Lazarus, 1988). The WCQ is one of the most widely used measures of parent coping (e.g., Aikens, Fischer, Namey, & Rudick, 1997; Folkman & Moskowitz, 2000; LaMontange & Pawlak, 1990; Pisula & Kossakowska, 2010).
The Early Childhood Environment Rating Scale – Revised (ECERS-R; Harms, Clifford, & Cryer, 1998) was used to measure quality of daycare. The ECERS-R appears to be the most frequently used measure of global quality in early childhood settings (Cassidy, Hestenes, Hegde, Hestenes, & Mims, 2005). It contains 43 items grouped into seven subscales: Personal Care Routines, Space and Furnishings, Language Reasoning, Activities, Program Structure, Interactions, and Parents and Staff. Cronbach’s alpha for the subscales ranged from .71 to .88 (Harms et al., 1998). For the present study, the Language Reasoning, Activities, Program Structure, and Interactions subscales were selected a priori as of most interest to examine in relation to executive functions. The ECERS-R data was collected as part of a larger study (Maggi, Roberts, MacLennan, & D’Angiulli, 2011) and the data was linked to the new data collected for the present study.
Data Analysis
Two-way repeated measures analyses of covariance (ANCOVAs) were carried out to test relationships between the level of executive functioning (median split “higher” versus “lower”), sex (boys, girls) and cortisol (across the three samples), with maternal education and parenting stress (PSI Parent Domain and PSI Life Stress) as covariates. Generalized linear modeling (GZLM) was performed to examine relationships between executive functions, cortisol, quality of daycare and parent coping, adjusted for parenting stress, mother education and child sex. Data analyses were carried out using SPSS version 18.
RESULTS
Participant Description
The characteristics of the sample are shown on Table 1. Parent participants were 97% mothers; the remaining 3% were primary caregiving fathers. Level of maternal education was used as a marker of socioeconomic status (SES). These families were from smaller cities and towns, not a major metropolitan area, and thereby represented generally lower SES, as 35% had 8th grade education or less. Only 10% were college graduates, and 2% had advanced education. Low education was not accounted for by immigration status, since 93% of the parents were born in Canada. Of the seven parents born outside Canada, all but one had resided there for more than 10 years, and four for more than 20 years.
Table 1.
All n = 101 |
Higher Global Executive Composite Score (Higher EF Problems) n = 50 |
Lower Global Executive Composite Score (Lower EF Problems) n = 51 |
||||
---|---|---|---|---|---|---|
Age (years) | Mean | SD | Mean | SD | Mean | SD |
|
|
|
||||
4.24 | 0.74 | 4.22 | 0.79 | 4.26 | 0.68 | |
|
|
|
||||
n | % | n | % | n | % | |
| ||||||
Children | ||||||
Sex | ||||||
Female | 53 | 52.5 | 26 | 52.0 | 27 | 52.9 |
Male | 48 | 47.5 | 24 | 48.0 | 24 | 47.1 |
Child Attends | ||||||
Daycare | 53 | 52.5 | 23 | 46.0 | 30 | 58.8 |
Preschool | 38 | 37.6 | 21 | 42.0 | 17 | 33.3 |
Kindergarten | 10 | 9.9 | 6 | 12.0 | 4 | 7.8 |
| ||||||
Age (years) | Mean | SD | Mean | SD | Mean | SD |
|
|
|
||||
34.25 | 5.01 | 34.11 | 6.55 | 34.83 | 5.45 | |
|
|
|
||||
n | % | n | % | n | % | |
| ||||||
Parents | ||||||
Relationship with child | ||||||
Mother | 98 | 97.0 | 49 | 98.0 | 49 | 96.1 |
Father | 3 | 3.0 | 1 | 2.0 | 2 | 3.9 |
Marital Status | ||||||
Married | 69 | 68.3 | 34 | 68.0 | 35 | 68.6 |
Single | 6 | 5.9 | 3 | 6.0 | 3 | 5.9 |
Divorced | 5 | 5.0 | 2 | 4.0 | 3 | 5.9 |
Widowed | 1 | 1.0 | 1 | 2.0 | 0 | 0.0 |
Separated | 9 | 8.9 | 5 | 10.0 | 4 | 7.8 |
Common Law | 11 | 10.9 | 5 | 10.0 | 6 | 11.8 |
Level of Education | ||||||
1st to 8th grade | 35 | 34.7 | 13 | 26.0 | 22 | 43.1 |
9th to 12th grade | 26 | 25.7 | 15 | 30.0 | 11 | 21.6 |
Vocational or some college | 28 | 27.7 | 16 | 32.0 | 12 | 23.5 |
College graduate | 10 | 9.9 | 6 | 12.0 | 4 | 7.8 |
Graduate or professional school | 2 | 2.0 | 0 | 0.0 | 2 | 3.9 |
Born in Canada | ||||||
Yes | 94 | 93.1 | 47 | 94.0 | 47 | 92.2 |
No | 7 | 6.9 | 3 | 6.0 | 4 | 7.8 |
Note. EF = executive functions.
Data Reduction
To reduce the number of measures from the WCQ, a principal components analysis (PCA) was conducted on the means of the scores of the eight scales of the WCQ. The PCA yielded two eigenvalues > 1 which were interpreted as a positive coping vector (eigenvalue 3.76, accounting for 47% of the variance) and a negative coping vector (eigenvalue 1.05, accounting for 13% of the variance), accounting for 60% of the variance overall. The loadings for each of the WCQ subscales on the two PCA components are shown in Table 2. Since Self-Control, Seeking Social Support, Planful Problem Solving, Positive Reappraisal and Distancing all loaded positively on component 1 and negatively on component 2, the first component was viewed as relatively positive coping and the second as relatively negative coping.
Table 2.
Ways of Coping Scales | Component
|
|
---|---|---|
1 | 2 | |
Confrontative Coping | .531 | .633 |
Self-Controlling Coping | .814 | −.029 |
Seeking Social Support | .512 | −.385 |
Accepting Responsibility | .782 | .140 |
Escape-Avoidance | .703 | .489 |
Planful Problem Solving | .609 | −.328 |
Positive Reappraisal | .789 | −.290 |
Distancing | .672 | −.208 |
Note. 96 parents completed the WCQ. The mean response for each of the eight scales was entered in the principal components analysis.
Cortisol, Executive Functions and Gender
Cortisol values are shown in Table 3. To examine the level of executive functioning in relation to cortisol and gender, median splits were applied to the BRIEF-P Global Executive Composite score and each Index score (Inhibitory Self-Control, Flexibility, and Emergent Metacognition; see Table 4). Two-way repeated measures ANCOVAs were carried out with cortisol across time as a repeated measures factor (Samples 1,2,3) and each executive function level (higher, lower) and sex (boys, girls) as between-subjects factors. There is a reported relationship between family context and child stress (Cutuli, 2012); consequently, in order to elucidate associations between cortisol and executive functions, we adjusted for mother education and parenting stress (PSI Parent Domain and PSI Life Stress) as covariates.
Table 3.
Sample | All
|
Higher Global Executive Composite Score (Higher EF Problems)
|
Lower Global Executive Composite Score (Lower EF Problems)
|
|||
---|---|---|---|---|---|---|
n = 101
|
n = 50
|
n = 51
|
||||
Mean | SD | Mean | SD | Mean | SD | |
1 | .127 | .06 | .135 | .06 | .118 | .05 |
2 | .121 | .06 | .126 | .06 | .117 | .05 |
3 | .108 | .04 | .110 | .04 | .106 | .04 |
Note. EF = executive functions. All cortisol samples were collected in the mid-to-late morning.
Table 4.
Questionnaire | All
|
Higher Global Executive Composite Score (Higher EF Problems)
|
Lower Global Executive Composite Score (Lower EF Problems)
|
||||||
---|---|---|---|---|---|---|---|---|---|
n = 101
|
n = 50
|
n = 51
|
|||||||
Range | Mean | SD | Range | Mean | SD | Range | Mean | SD | |
BRIEF-P* | |||||||||
Inhibitory Self-Control Index score | 35–90 | 49.11 | 10.15 | 44–90 | 56.54 | 8.99 | 35–51 | 41.82 | 4.20 |
Flexibility Index score | 35–92 | 49.15 | 10.17 | 40–92 | 55.08 | 10.57 | 35–57 | 43.33 | 5.26 |
Emergent Metacognition Index score | 33–90 | 49.38 | 10.89 | 42–90 | 57.74 | 9.34 | 33–49 | 41.18 | 3.61 |
Global Executive Composite score | 33–91 | 49.03 | 10.96 | 47–91 | 57.42 | 9.51 | 33–46 | 40.80 | 3.52 |
PSI* | |||||||||
Parent Domain | 58–192 | 114.98 | 23.39 | 77–192 | 123.98 | 24.71 | 58–160 | 106.16 | 18.32 |
Life Stress | 0–53 | 11.23 | 9.95 | 0–53 | 11.96 | 11.09 | 0–32 | 10.51 | 8.73 |
ECERS-R | |||||||||
Language Reasoning | 4.25–6.75 | 5.91 | 0.75 | 4.25–6.75 | 5.77 | 0.80 | 4.25–6.75 | 6.05 | 0.69 |
Activities | 3.88–6.10 | 5.17 | 0.69 | 3.88–6.10 | 5.19 | 0.70 | 3.88–6.00 | 5.16 | 0.69 |
Program Structure | 5.66–7.00 | 6.58 | 0.40 | 5.66–7.00 | 6.60 | 0.43 | 5.66–7.00 | 6.57 | 0.37 |
Interactions | 4.40–7.00 | 6.58 | 0.29 | 4.40–7.00 | 6.52 | 0.36 | 6.20–7.00 | 6.63 | 0.19 |
| |||||||||
n = 96
|
n = 48
|
n = 48
|
|||||||
Range | Mean | SD | Range | Mean | SD | Range | Mean | SD | |
| |||||||||
WCQ* (relative scores) | |||||||||
Confrontative Coping | 0–0.54 | 0.13 | 0.08 | 0–0.28 | 0.12 | 0.62 | 0–0.54 | 0.14 | 0.09 |
Distancing | 0–0.25 | 0.10 | 0.06 | 0–0.24 | 0.10 | 0.06 | 0–0.25 | 0.10 | 0.06 |
Self-Controlling Coping | 0.03–0.29 | 0.15 | 0.05 | 0.03–0.29 | 0.15 | 0.05 | 0.03–0.25 | 0.14 | 0.05 |
Seeking Social Support | 0–0.47 | 0.16 | 0.09 | 0–0.44 | 0.16 | 0.09 | 0.02–0.47 | 0.16 | 0.10 |
Accepting Responsibility | 0–0.25 | 0.10 | 0.07 | 0–0.25 | 0.11 | 0.06 | 0–0.23 | 0.09 | 0.07 |
Escape-Avoidance | 0–0.20 | 0.07 | 0.05 | 0–0.19 | 0.78 | 0.05 | 0–0.20 | 0.07 | 0.05 |
Planful Problem Solving | 0–0.52 | 0.18 | 0.08 | 0.04–0.34 | 0.17 | 0.06 | 0–0.52 | 0.19 | 0.10 |
Positive Reappraisal | 0–0.28 | 0.11 | 0.05 | 0–0.28 | 0.10 | 0.06 | 0–0.25 | 0.11 | 0.05 |
Note.
Questionnaire completed by parent. EF = executive functions.
Global Executive Composite
Cortisol levels did not differ across samples (F[2, 188] < 1, p = .67). Children with lower executive functions had significantly higher cortisol levels (F[1, 94] = 4.44, p = .038). Children with higher child cortisol had parents with greater parenting stress (F[1, 94] = 6.32, p = .014), but not life stress (F[1, 94] < 1, p = .48), or maternal education (F[1, 94] = 1.38, p = .24). Sex was not significant (F[1, 94] = 2.07, p = .15). No interaction effects were statistically significant (each p > .41). Cortisol in relation to the level of child global executive function is shown in Figure 1.
Inhibitory Self-Control
Cortisol levels did not differ across the samples (F[2, 188] < 1, p = .60), and did not differ by level of inhibitory self-control (F[1, 94] = 1.73, p = .19). Children with higher child cortisol also had parents with higher parenting stress (F[1, 94] = 5.04, p = .027), but not life stress (F[1, 94] < 1, p = .52), or maternal education (F[1, 94] = 1.85, p = .18). Gender was not significant (F[1, 94] = 1.97, p = .16). No interaction effects were statistically significant (each p > .36).
Flexibility
Cortisol levels did not differ across the samples (F[2, 188] < 1, p = .58). Cortisol levels trended toward a relationship with higher, as compared with lower, flexibility scores (F[1, 94] = 3.72, p = .057). Children with higher child cortisol also had parents with higher parenting stress (F[1, 94] = 6.24, p = .014), but not life stress (F[1, 94] = 1.14, p = .29) or maternal education (F[1, 94] = 1.89, p = .17). Sex was not significant (F[1, 94] = 1.36, p = .25). No interaction effects were statistically significant (each p > .34).
Emergent Metacognition
Cortisol levels did not differ across the samples (F[2, 188] < 1, p = .55). Children with poorer emergent metacognition had a trend towards higher cortisol levels (F[1, 94] = 2.87, p = .094). Children with higher child cortisol also had parents with higher parenting stress (F[1, 94] = 5.27, p = .024), but not life stress (F[1, 94] = < 1, p = .56), or maternal education (F[1, 94] = 1.43, p = .24). Sex was not significant (F[1, 94] = 1.69, p = .20). No interaction effects were statistically significant (each p > .29).
Executive Functions in relation to Quality of Daycare and Parent Coping
To examine the relationships between executive functions, cortisol, quality of day-care and parent coping, adjusted for parenting stress, maternal education and sex, GZLM was performed following the GENLIN procedure in SPSS 18 that permits examination of effects with non-independent measures and potential confounders. Since the ANCOVAs above showed no difference in cortisol levels across the three samples, the average cortisol level was used in all further analyses. The Positive and Negative parent coping scores generated from the PCA above were used in the GENLIN analyses. Each outcome measure (BRIEF-P Global Executive Composite, Inhibitory Self-Control, Flexibility, and Emergent Metacognition Index scores) was entered as a continuous measure.
Global Executive Composite
The omnibus test of the model was significant (χ2[11] = 47.40, p < .001), suggesting that further interpretation of variables was appropriate. Children with lower executive functions differed from children with higher executive functions in that the lower executive functions children trended toward higher cortisol (χ2[1] = 3.43, p < .064), and had lower maternal education (χ2[11] = 5.59, p < .018), higher parenting stress (χ2[11] = 29.69, p < .001), and lower quality daycare/preschool for the language reasoning domain (χ2[11] = 3.83, p < .050). In contrast, no differences were found for child sex, life stress, parenting coping, or daycare/preschool quality for the activities, interaction and program structure domains.
Inhibitory Self-Control
The omnibus test of the model was significant (χ2[11] = 45.91, p < .001), suggesting that further interpretation of variables was appropriate. Children with lower executive functions differed from children with higher executive functions in that the lower executive functions children trended toward higher cortisol (χ2[1] = 3.31, p < .069), higher parent life stress (χ2[11] = 2.92, p < .088), and lower quality of daycare on the interaction domain (χ2[11] = 2.75, p < .098). In addition, lower executive functions children had lower maternal education (χ2[11] = 5.55, p < .018), higher parenting stress (χ2[11] = 25.55, p < .001), and less daycare quality for the language reasoning domain (χ2[11] = 3.83, p < .050). In contrast, no differences were found for child sex, parenting coping, or daycare quality for the activities or program structure domains.
Flexibility
The omnibus test of the model was significant (χ2[11] = 51.51, p < .001), suggesting that further interpretation of variables was appropriate. Children with lower executive functions differed from children with higher executive functioning in that the lower executive functions children had higher cortisol (χ2[1] = 7.23, p < .007), higher parenting stress (χ2[11] = 36.48, p < .001), and higher parent life stress (χ2[11] = 5.48, p < .019). In contrast, no differences were found for child sex, maternal education, parent coping, or daycare/preschool quality for any domain.
Emergent Metacognition
The omnibus test of the model was significant (χ2[11] = 34.49, p < .001) suggesting that further interpretation of variables was appropriate. Children with lower executive functions had mothers with lower maternal education (χ2[11] = 4.51, p < .034) and higher parenting stress (χ2[11] = 23.27, p < .001) relative to children with higher executive functions. In contrast, no differences were found for child sex, cortisol level, parent life stress, parent coping, or daycare quality for any domain.
DISCUSSION
Our primary finding was that children with poorer overall executive functioning had higher salivary cortisol levels, and their parents self-reported higher parenting stress. These results were consistent across domains of executive functioning using an ecologically valid measure of parent-reported child executive functioning (Gioia et al., 2003). However, this relationship between poorer executive functioning and higher cortisol appeared particularly compelling for children with lower scores for Flexibility. We found no differences in child executive functioning in relation to child sex.
Further, when maternal education, parent coping and daycare quality were included in the model, there was a trend suggesting that children with less Inhibitory Self-Control and Flexibility may also have parents with higher life stress. While only a trend was revealed, this may suggest that, when coping skills and other confounding factors are accounted for, parents of children with poor self-control and flexibility experience greater parenting stress, and that this parenting stress may become an aspect of increased life stress overall. Finally, for children with poor Inhibitory Self-Control, reduced language reasoning and other effects related to poor daycare quality were evident.
Our results, using the BRIEF-P as a measure of everyday executive functioning, are generally in agreement with previous literature that has utilized direct testing of child executive functions. Specifically, we found that children with lower executive functioning also had higher rates of salivary cortisol, consistent with Maldonado et al. (2008), and that salivary cortisol varied as a function of behavioral measures of executive functioning, which can perhaps equate to a proxy for early school adjustment (Blair et al., 2005; Miller & Cohen, 2001). Moreover, the present study confirms and extends previous work that found a relationship between parenting stress and child executive functioning (McLuckie, 2013), and our present findings in a sample of preschool-age children from the general population support the previous link between parenting stress and child cortisol that we reported in infants born very prematurely (Tu et al., 2007). However, unlike the findings of Geoffroy et al. (2006) and Alwin (2006), we found minimal differences in cortisol levels as a function of daycare/preschool quality; however, those studies found an effect in the late afternoon whereas we examined cortisol only earlier in the day.
Limitations
The cross-sectional nature of our data restricts our ability to interpret the directionality of our findings as to whether parent stress results in increased child cortisol, whether increased child cortisol results in greater parent stress, or whether this relationship is bidirectional. Similarly, we are unable to determine the directionality for the impacts of poor executive functions. It may be that lower child executive functioning contributes to family stress, family stress contributes to lower executive functioning, or both. Future longitudinal research will be necessary in order to determine the directionality of such relationships. Other limitations were the lack of additional corroborating data to supplement parent-report questionnaires, such as teacher report of child executive functions.
Conclusion
The current study contributed to understanding executive functioning in pre-school children as it relates to child salivary cortisol and parenting stress. The present findings, in combination with previous research, suggest the importance of promoting child executive functioning skills as a means of decreasing child and parenting stress. Our data provide associations; therefore, it is hard to determine whether the higher child cortisol levels are a result of greater parenting stress, or whether higher cortisol levels are an inherent aspect of poor executive functioning and present regardless of parenting stress levels. Cutuli’s (2012) work suggests that higher child cortisol levels were only found when in the actual presence of a harsh or hostile caregiver. Consequently, one possibility is that raising a child who displays low flexibility may lead to increased parenting stress, in turn increasing the possibility for increased harshness or hostility in parenting, and subsequently higher rates of child stress, as reflected via salivary cortisol. An equally plausible possibility is that there may be joint similarities in parent and child characteristics. Future studies would benefit from including more measures of parent factors, such as maternal and paternal cognitive flexibilty and cortisol levels to elucidate these parent-child relationships.
Recent perspectives on environmental contributions to executive functioning provide hope for techniques to train executive functioning generally, similar to more established methods in training specific skills such as attention and memory. For example, Harvard University’s Center on the Developing Child has created a series of working papers regarding the development of executive functioning in early childhood (Center on the Developing Child at Harvard University, 2011). It is proposed that through training, as any other learned skill, increased executive functioning can lead to improved parent and child outcomes, including reduced stress and cortisol (Diamond, Barnett, Thomas, & Munro, 2007). Future research should continue to elucidate the links among these important variables in the child-parent dyad and consider new and innovative approaches to improving executive functions skills and development throughout early childhood.
Acknowledgments
The authors would like to thank the families and teachers that contributed their time to this project.
This work was supported by the Human Early Learning Partnership and is dedicated to the late Clyde Hertzman.
Footnotes
No potential conflict of interest was reported by the authors.
References
- Abidin R. Parenting stress index. 3. Odessa, FL: Psychological Assessment Resources; 1995. [Google Scholar]
- Aikens JE, Fischer JS, Namey M, Rudick RA. A replicated prospective investigation of life stress, coping, and depressive symptoms in multiple sclerosis. Journal of Behavioral Medicine. 1997 Oct;20(5):433–445. doi: 10.1023/A:1025547431847. [DOI] [PubMed] [Google Scholar]
- Alexander M, Stuss D. Frontal injury: Impairments of fundamental processes lead to functional consequences. Journal of the International Neuropsychological Society. 2006;12:192–193. doi: 10.1017/S1355617706060292. [DOI] [PubMed] [Google Scholar]
- Alwin J. Salivary cortisol in infants at daycare and at home. Dissertation Abstracts International: Section B: the Sciences and Engineering. 2006;66(9-B):5119. [Google Scholar]
- Anderson V. Assessing executive functions in children: Biological, psychological, and developmental considerations. Pediatric Rehabilitation. 2001;4(3):119–136. doi: 10.1080/13638490110091347. [DOI] [PubMed] [Google Scholar]
- Anderson VA, Anderson P, Northam E, Jacobs R, Mikiewicz O. Relationship between cognitive and behavioral measures of executive function in children with brain disease. Child Neuropsychology. 2002;8:231–240. doi: 10.1076/chin.8.4.231.13509. [DOI] [PubMed] [Google Scholar]
- Bechara A, Van Der Linden M. Decision making an impulse of control after frontal lobe injuries. Current Opinion in Neurology. 2005;18:734–739. doi: 10.1097/01.wco.0000194141.56429.3s. [DOI] [PubMed] [Google Scholar]
- Blair C, Granger D, Peters Razza R. Cortisol reactivity is positively related to executive function in preschool children attending Headstart. Child Development. 2005 May-Jun;76(3):554–567. doi: 10.1111/cdev.2005.76.issue-3. [DOI] [PubMed] [Google Scholar]
- Blair C, Razza RP. Relating effortful control, executive function and false belief understanding to emerging math and literacy ability in kindergarten. Child Development. 2007 Mar;78(2):647–663. doi: 10.1111/cdev.2007.78.issue-2. [DOI] [PubMed] [Google Scholar]
- Brummelte S, Grunau RE, Synnes AR, Whitfield MF, Petrie-Thomas J. Declining cognitive development from 8 to 18 months in preterm children predicts persisting higher parenting stress. Early Human Development. 2011 Apr;87(4):273–280. doi: 10.1016/j.earlhumdev.2011.01.030. [DOI] [PubMed] [Google Scholar]
- Bull R, Espy KA, Wiebe SA. Short-term memory, working memory, and executive functioning in preschoolers: Longitudinal predictors of mathematical achievement at age 7 years. Developmental Neuropsychology. 2008;33(3):205–228. doi: 10.1080/87565640801982312. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cassidy DJ, Hestenes LL, Hegde A, Hestenes S, Mims S. Measurement of quality in preschool childcare classrooms: An exploratory and confirmatory factor analysis of the early childhood environment rating scale-revised. Early Childhood Research Quarterly. 2005;20(3):345–360. doi: 10.1016/j.ecresq.2005.07.005. [DOI] [Google Scholar]
- Center on the Developing Child at Harvard University. Building the brain’s “air traffic control” system: How early experiences shaped the development of executive function. 2011 Working paper number 11 Retrieved from www.developingchild.harvard.edu.
- Chen FR, Raine A, Soyfer A, Granger D. Interaction of adrenocortical activity and autonomic arousal on childrens’ externalizing and internalizing behavior problems. Journal of Abnormal Child Psychology. 2015;43(1):189–202. doi: 10.1007/s10802-014-9900-y. [DOI] [PubMed] [Google Scholar]
- Clark CA, Pritchard VE, Woodward LJ. Preschool executive functioning abilities predict early mathematics achievement. Developmental Psychology. 2010 Sep;46(5):1176–1191. doi: 10.1037/a0019672. [DOI] [PubMed] [Google Scholar]
- Collett BR, Cloonan YK, Speltz ML, Anderka M, Werler MM. Psychosocial functioning in children with and without orofacial clefts and their parents. The Cleft Palate Craniofacial Journal. 2012 Jul;49(4):397–405. doi: 10.1597/10-007. [DOI] [PubMed] [Google Scholar]
- Cutuli JJ. Context, cortisol, and executive functions among children experiencing homelessness. Dissertation Abstracts International: Section B: the Sciences and Engineering. 2012;73(1-B):659. [Google Scholar]
- Denckla MB. The behavior rating inventory of executive function: Commentary. Child Neuropsychology. 2002;8(4):304–306. doi: 10.1076/chin.8.4.304.13512. [DOI] [PubMed] [Google Scholar]
- Diamond A. The early development of executive functions. In: Bialystok E, Craik FI, editors. Lifespan cognition: Mechanisms of change. New York, NY: Oxford University press; 2006. pp. 70–95. [Google Scholar]
- Diamond A, Barnett WS, Thomas J, Munro S. The early years: Preschool program improves cognitive control. Science. 2007;318:1387–1388. doi: 10.1126/science.1151148. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ellis M, Weiss B, Lochman J. Executive functions in children: Associations with aggressive behavior and appraisal processing. Journal of Abnormal Child Psychology. 2009;37:945–956. doi: 10.1007/s10802-009-9321-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elzinga Bernet M, Bakker A, Bremner D. Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall. Psychiatry Researcher. 2005;134:211–223. doi: 10.1016/j.psychres.2004.11.007. [DOI] [PubMed] [Google Scholar]
- Espy KA. Using developmental, cognitive, and neuroscience approaches to understand executive control in young children. Developmental Neuropsychology. 2004;26(1):379–384. doi: 10.1207/s15326942dn2601_1. [DOI] [PubMed] [Google Scholar]
- Faught J, Bierl C, Barton B, Kemp A. Stress in mothers of young children with eczema. Archives of Disease in Childhood. 2007 Aug;92(8):683–686. doi: 10.1136/adc.2006.112268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fite P, Stoppelbein L, Greening L. Parenting stress as a predictor of age upon admission to a child psychiatric inpatient facility. Child Psychiatry and Human Development. 2008;39(2):171–183. doi: 10.1007/s10578-007-0080-7. [DOI] [PubMed] [Google Scholar]
- Folkman S, Lazarus R. Manual for the ways of coping questionnaire. Paulo Alto, CA: Consulting Psychologists Press; 1988. [Google Scholar]
- Folkman S, Moskowitz JT. Positive affect and the other side of coping. American Psychologist. 2000 Jun;55(6):647–654. doi: 10.1037/0003-066X.55.6.647. [DOI] [PubMed] [Google Scholar]
- Ganesalingam K, Yeates KO, Taylor HG, Walz NC, Stancin T, Wade S. Executive functions and social competence in young children 6 months following traumatic brain injury. Neuropsychology. 2011 Jul;25(4):466–476. doi: 10.1037/a0022768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geoffroy MC, Cote SM, Parent S, Seguin JR. Daycare attendance, stress, and mental health. Canadian Journal of Psychiatry. 2006 Aug;51(9):607–615. doi: 10.1177/070674370605100909. [DOI] [PubMed] [Google Scholar]
- Gioia GA, Espy KA, Isquith PK. Behavior rating inventory of executive function: Preschool version. Lutz, FL: Psychological Assessment Resources; 2003. [Google Scholar]
- Gioia GA, Isquith PK. Ecological assessment of executive function in traumatic brain injury. Developmental Neuropsychology. 2004;25:135–158. doi: 10.1080/87565641.2004.9651925. [DOI] [PubMed] [Google Scholar]
- Gioia GA, Isquith PK, Guy SC, Kenworthy L. Assessment of executive function in children with neurological impairments. In: Simeonsson R, Rosenthal S, editors. Psychological and developmental assessment. New York, NY: The Guilford Press; 2001. pp. 317–350. [Google Scholar]
- Glenn S, Cunningham C, Poole H, Reeves D, Weindling M. Maternal parenting stress and its correlates in families with a young child with cerebral palsy. Child: Care, Health and Development. 2009;35(1):71–78. doi: 10.1111/j.1365-2214.2008.00891.x. [DOI] [PubMed] [Google Scholar]
- Gunnar MR, Bruce J, Hickman SE. Salivary cortisol response to stress in children. Advances in Psychosomatic Medicine. 2001;22:52–60. doi: 10.1159/000059275. [DOI] [PubMed] [Google Scholar]
- Harms T, Clifford R, Cryer D. Early childhood environment rating scale-revised. New York, NY: Teachers College; 1998. [Google Scholar]
- Hostinar CE, Johnson AE, Gunnar MR. Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Developmental Science. 2015;18(2):281–297. doi: 10.1111/desc.12195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isquith PK, Gioia GA, Espy KA. Executive function in preschool children: Examination through everyday behavior. Developmental Neuropsychology. 2004;26(1):403–422. doi: 10.1207/s15326942dn2601_3. [DOI] [PubMed] [Google Scholar]
- LaMontange LL, Pawlak R. Stress and coping of parents of children in a pediatric intensive care unit. Heart and Lung. 1990 Jul;19(4):416–421. [PubMed] [Google Scholar]
- Lupien SJ, Fiocco A, Wan N, Maheu F, Lord C, Schramek T, Tu MT. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology. 2005 Apr;30(3):225–242. doi: 10.1016/j.psyneuen.2004.08.003. [DOI] [PubMed] [Google Scholar]
- Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE. The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and Cognition. 2007 Dec;65(3):209–237. doi: 10.1016/j.bandc.2007.02.007. [DOI] [PubMed] [Google Scholar]
- Maggi S, Roberts W, MacLennan D, D’Angiulli A. Community resilience, quality childcare, and preschoolers’ mental health: A three-city comparison. Social Science & Medicine. 2011;73(7):1080–1087. doi: 10.1016/j.socscimed.2011.06.052. [DOI] [PubMed] [Google Scholar]
- Mahone EM, Hoffman J. Behavior ratings of executive function among preschoolers with ADHD. The Clinical Neuropsychologist. 2007;21(4):569–586. doi: 10.1080/13854040600762724. [DOI] [PubMed] [Google Scholar]
- Mahone EM, Cirino PT, Cutting LE, Cerrone PM, Hagelthorn KM, Hiemenz JR, … Denkla MB. Validity of the behavior rating inventory of executive function in children with ADHD and/or Tourette syndrome. Archives of Clinical Neuropsychology. 2002;17:643–662. [PubMed] [Google Scholar]
- Maldonado EF, Fernandez FJ, Trianes MV, Wesnes K, Petrini O, Zangara A, Ambrosetti L. Cognitive performance and morning levels of salivary cortisol and α-amylase in children reporting high vs. low daily stress perception. The Spanish Journal of Psychology. 2008 May;11(1):3–15. doi: 10.1017/S1138741600004066. [DOI] [PubMed] [Google Scholar]
- McCandless S, O’Laughlin L. The clinical utility of the Behavior Rating Inventory of executive function (BRIEF) in the diagnosis of ADHD. Journal of Attention Disorders. 2007;10:381–389. doi: 10.1177/1087054706292115. [DOI] [PubMed] [Google Scholar]
- McClelland MM, Morrison FJ, Holmes DL. Children at risk for early academic problems: The role of learning-related social skills. Early Childhood Research Quarterly. 2000;15(3):307–329. doi: 10.1016/S0885-2006(00)00069-7. [DOI] [Google Scholar]
- McCormick CM, Lewis E, Somley B, Kahan TA. Individual differences in cortisol levels and performance on a test of executive function in men and women. Physiology & Behavior. 2007;91:87–94. doi: 10.1016/j.physbeh.2007.01.020. [DOI] [PubMed] [Google Scholar]
- McLuckie A. Are executive function difficulties reported by parents and teachers associated with elevated levels of parenting stress for children diagnosed with attention deficit hyper-activity disorder, with and without oppositional defiant disorder? Dissertation Abstracts International: Section B: The Sciences and Engineering. 2013;73:7–B(E). [Google Scholar]
- Miller GE, Chen E, Zhou ES. If it goes up, must it come down? Chronic stress and the hypothalamic–pituitary–adrenocortical axis in humans. Psychological Bulletin. 2007;133:25–45. doi: 10.1037/0033-2909.133.1.25. [DOI] [PubMed] [Google Scholar]
- Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annual Review of Neuroscience. 2001 Mar 1;24(1):167–202. doi: 10.1146/annurev.neuro.24.1.167. [DOI] [PubMed] [Google Scholar]
- Pisula E, Kossakowska Z. Sense of coherence and coping with stress among mothers and fathers of children with autism. Journal of Autism and Developmental Disorders. 2010 Dec;40(12):1485–1494. doi: 10.1007/s10803-010-1001-3. [DOI] [PubMed] [Google Scholar]
- Plessow F, Schade S, Kirschbaum C, Fischer R. Better not to deal with two tasks at the same time when stressed? Acute psychosocial stress reduces task shielding in dual-task performance. Cognitive, Affective, & Behavioral Neuroscience. 2012 Sep;12(3):557–570. doi: 10.3758/s13415-012-0098-6. [DOI] [PubMed] [Google Scholar]
- Quas JA, Bauer A, Boyce WT. Physiological reactivity, social support, and memory in early childhood. Child Development. 2004;75(3):797–814. doi: 10.1111/cdev.2004.75.issue-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raaijmakers M, Smidts D, Sergeant J, Maassen G, Posthumus J, Van Engeland H, Matthys W. Executive functions in preschool children with aggressive behavior: Impairments in inhibitory control. Journal of Abnormal Child Psychology. 2008;36:1097–1107. doi: 10.1007/s10802-008-9235-7. [DOI] [PubMed] [Google Scholar]
- Sharpley CF, Bitsika V, Efremidis B. Influence of gender, parental health, and perceived expertise of assistance upon stress, anxiety, and depression among parents of children with autism. Journal of Intellectual and Developmental Disability. 1997;22(1):19–28. doi: 10.1080/13668259700033261. [DOI] [Google Scholar]
- Starcke K, Wolf OT, Markowitsch HJ, Brand M. Anticipatory stress influences decision-making under explicit risk conditions. Behavioral Neuroscience. 2008 Dec;122(6):1352–1360. doi: 10.1037/a0013281. [DOI] [PubMed] [Google Scholar]
- Stawski RS, Almeida DM, Lachman ME, Tun PA, Rosnick CB, Seeman T. Associations between cognitive function and naturally occurring daily cortisol during middle adulthood: Timing is everything. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences. 2011 Jul;66B(Suppl 1):i71–i81. doi: 10.1093/geronb/gbq094. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tu MT, Grunau RE, Petrie-Thomas J, Haley DW, Weinberg J, Whitfield MF. Maternal stress and behavior modulate relationships between neonatal stress, attention, and basal cortisol at 8 months in preterm infants. Developmental Psychobiology. 2007 Mar;49(2):150–164. doi: 10.1002/dev.20204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vermeer HJ, van Ijzendoorn MH. Children’s elevated cortisol levels at daycare: A review and meta-analysis. Early Childhood Research Quarterly. 2006;21(3):390–401. doi: 10.1016/j.ecresq.2006.07.004. [DOI] [Google Scholar]
- Webster RI, Majnemer A, Platt RW, Shevell MI. Child health and parental stress in school-age children with a preschool diagnosis of developmental delay. Journal of Child Neurology. 2008;23(1):32–38. doi: 10.1177/0883073807307977. [DOI] [PubMed] [Google Scholar]