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. Author manuscript; available in PMC: 2023 Jan 1.
Published in final edited form as: Psychoneuroendocrinology. 2021 Oct 29;135:105578. doi: 10.1016/j.psyneuen.2021.105578

Pubertal Stress Recalibration and Later Social and Emotional Adjustment Among Adolescents: The Role of Early Life Stress

Nicole B Perry 1, Bonny Donzella 2, Megan R Gunnar 2
PMCID: PMC8751423  NIHMSID: NIHMS1754012  PMID: 34741981

Abstract

The current study investigated whether recalibration of the hypothalamic-pituitary - adrenocortical (HPA) axis stress response in youth who had previously experienced early life stress (ELS) would predict socioemotional adjustment in a follow-up assessment approximately 2–4 years later when youth were 12- to 21-years old. The sample consisted of previously institutionalized (PI) (N=96) youth and a comparison non-adopted (NA) group (N=117). Youth were 16 years old on average at the time of the follow-up assessment. Parent and youth-reported measures were used to assess youth‟s internalizing symptoms and emotion regulation. Parent-reported measures were used to assess youth‟s externalizing symptoms. We tested whether showing cortisol increases (vs. not) across the peripubertal period was associated with later social and emotional adjustment differently for PI and NA youth. Significant interactions emerged showing that for PI youth only, increases in cortisol reactivity across the peripubertal period was associated with poorer subsequent socioemotional functioning.

Keywords: adolescence, cortisol, HPA, institutionalized, social functioning, emotional adjustment, recalibration

A substantial amount of research has investigated the negative effects of early institutional care on child development and has made clear that early life stress characterized by little caregiver interaction and low responsiveness is associated with altered brain architecture and atypical biobehavioral functioning (Nelson, Zeanah, & Fox, 2007; Sonuga-Barke et al., 2017; van IJzendoorn et al., 2020). The development of children‟s hypothalamic-pituitary - adrenal (HPA) axis has been of interest to developmental scientists given its role in stress response and regulation. Multiple studies suggest that early institutional care alters the HPA axis‟ cortisol stress response such that children demonstrate blunted cortisol reactivity to stress, or hypocortisolism, following early institutionalization (Struber, Stuber, & Roth, 2014; Koss, Mliner, Donzella, & Gunnar, 2016; however, see also Gunnar, Frenn, Wewerka, & Van Ryzin, 2009). McLaughlin and colleagues (2015), for example, showed evidence of a causal link between early institutional care and blunted HPA axis reactivity; children removed from institutional care and placed in supportive homes before 2 years of age responded comparably to never institutionalized children, while those placed after 2 years of age showed a lack of response, similar to those who remained in care as usual.

Although too much or prolonged cortisol activation can lead to poor health outcomes (Fries, Hesse, Hellhammer, & Hellhammer, 2005), acute cortisol stress responding is necessary for adaptive functioning; a blunted or non-existent cortisol stress response leaves children with fewer physiological resources to adequately cope with environmental threat or challenge. Thus, developmental scientists have used blunted stress reactivity as an indicator of early risk and as a predictor of social and emotional behavioral disorders in children and adolescents (e.g., Alink et al., 2008; Alink, Cicchetti, Kim, & Rogosch, 2012; DePasquale, Lawler, Koss, & Gunnar, 2020; Ouellet-Morin et al., 2011). Given the established association between hypocortisolism and institutional care, it is not surprising that previously-institutionalized (PI) youth have also been found to experience poorer mental health, greater emotional problems, and psychopathology, including both internalizing (Bos et al., 2011; Colvert et al., 2008; Wiik et al., 2010; Zeanah et al., 2009) and externalizing symptoms (Bos et al., 2011; Hawk & McCall, 2010; Merz & McCall, 2010; Wiik et al., 2010), compared to their non-adopted (NA) peers. However, empirical work directly examining the association between cortisol reactivity to stress and concurrent or future social, emotional, and behavior problems in PI youth is scarce. In one study, Koss and colleagues (2016) showed that hypocortisolism during toddlerhood served as a mediator between early institutional care and teacher-reported attention and externalizing problems during kindergarten. Researchers have also found evidence of a developmental cascade from institutional care, to blunted cortisol reactivity to poorer social competences and peer difficulties (DePasquale et al., 2020; Pitula, DePasquale, Mliner, & Gunnar, 2019).

Importantly, much of this research is conducted during childhood and does not account for potential developmental changes that may occur across the adolescent period. Chronic stress and activation while in institutional care during infancy provides the environmental context in which the HPA axis develops, likely resulting in a down-regulation of HPA activity and the blunted cortisol stress response patterns that are commonly observed in PI children. As youth transition through puberty, a time characterized by physical and hormonal changes initiated and controlled by the neural and endocrine systems that interact with the HPA axis (Dismukes et al., 2015), the HPA axis may recalibrate to reflect the current environmental conditions in which youth now live. Empirical work (King et al., 2016; Quevedo, Johnson, Loman, LaFavor, & Gunnar, 2012), including recent research using the same sample as the current study, has supported this hypothesis. Specifically, in a cross-sectional analysis, it was shown that PI youth who were in the early stages of puberty displayed blunted HPA axis reactivity to a social stressor compared to NA children, but PI children who were categorized as being in mid to late puberty showed cortisol reactivity similar to that of their NA counterparts (DePasquale et al., 2019). In a follow-up longitudinal investigation, data showed within-individual increases in pubertal stage were associated with increases in cortisol stress reactivity for PI youth but not NA youth (Gunnar et al., 2019). Importantly, the increases in cortisol reactivity corresponding with pubertal stage in the PI youth resulted in cortisol stress responses that were comparable to the NA youth who had never experienced early life stress.

The next logical question was whether the increases in cortisol that were observed across the peripubertal period in previous work were associated with changes in emotional and behavioral functioning; if cortisol reactivity increases to more normative levels, does this correspond to decreases in behavioral and emotional problems associated with early institutional care? To address this question, we examined the bidirectional associations between increases in PI youths‟ cortisol stress reactivity and changes in internalizing symptoms, externalizing symptoms, and social behavior across 3 time points during the adolescent period (Perry et al., 2020, 2021). Analyses revealed no associations between cortisol reactivity and externalizing symptoms. However, increases in cortisol reactivity predicted subsequent increases in internalizing symptoms and socially anxious behavior for PI youth across the first three assessments during late childhood and adolescence. Thus, the results suggested that recalibrating to more normative levels of cortisol stress responding might contribute to increasing, rather than decreasing, emotional symptoms in youth with histories of early life stress.

In the current study, we questioned whether PI youth who had previously showed increases in cortisol stress reactivity over the peripubertal period would eventually adapt to their more normally reactive stress response systems. If so, they may no longer show positive associations between earlier increases in cortisol stress responses and measures of anxiety and depression when measured years later. However, it is also possible that the association between cortisol increases over the peripubertal period and internalizing symptoms would remain, suggesting that developing a more typically reactive HPA axis may contribute to a more emotionally reactive neurobiological system. Because there is evidence that PI youth who have been adopted from institutions into supportive homes show increases in emotional and behavioral problems during adolescence (Sonuga-Barke et al., 2017), we predicted that recalibration of the axis earlier during pubertal development would be predictive of heightened emotional problem symptoms for PI youth. NA youth were not expected to show this effect as their emotion systems had developed in the context of a normally reactive HPA axis.

Method

Participants

Participants in the current study were initially part of a short-term accelerated longitudinal study examining the association between puberty and stress reactivity in children who experienced early institutional care. As part of the original study, measures were obtained at each session, and three sessions occurred over the span of 2 years, with approximately 1 year between visits (M=12.23 mo, SD = .90 mo). The current and 4th wave of collection took place between 2–4 years after the last in-person assessment (M=3.4 yr SD=.69, range 1.9–4.6 yr later), when participants were 12–21 years of age (M=16.47 yr, SD=2.35 yr).

At study onset, the sample consisted of 310 children; 124 (84 female) children were adopted internationally from institutional (i.e., orphanage) care (post-institutionalized, PI) into the United States of America, and 172 (90 female) children were non-adopted (NA) and had been born and raised with their biological families. Both groups were raised in the same Midwestern state. PI children spent at least 50% of their pre-adoption lives in institutionalized care, versus foster care or other arrangements (M= 95%, range 50 to 100%). Age at adoption ranged from 5.5 months to 57 months (M = 18.5 mo, SD = 11.65). The children ranged from 7.08 to 15.12 years at the initial time of testing, with mean ages not differing for the two groups (Mpi =11.3 yr, SD = 2.4yr; Mna =11.2 yr, SD = 2.3 yr, t(294)=.42, ns). The mean family income for the two groups also did not differ (χ2(7) = 11.6, p = .11) and was $100,000-$150,000 per year. Parental education did not differ between groups, with over 75% of the parents in both groups having a four-year college degree or higher. Parents reported that 90% of NA youth were White, 7.6% were more than one race, 2% were Black, African, or African American, and .6% were Asian. In contrast, 40% of the PI children were White, 41% were Asian, 10.5% indigenous to the Americas, 5% Black or African, and 3.3% were of more than one race. Regarding country of birth, 38% of PI youth were adopted from Russia, 21% from China, 10.5% from India, and 6.5% from Guatemala, 4.8% from Ukraine, 4% from Colombia, 4% from Vietnam, 2.4% from Kazakhstan, and 8.9% from other countries including: Ecuador, Ethiopia, Haiti, Nepal, Philippines, and Slovakia. The racial distribution of the parents in both groups did not differ and was overwhelmingly white.

By the third in-person visit, the sample had reduced to 238 or 77% of the original sample, and the attrition did not result in differences in sample characteristics described above. For the 4th wave of data collection, the full sample was approached for participation, and 215 (69% of the original sample, 90% of the third wave) responded (parent N=215, child N=204). Of the 215 respondents, 164 (PI = 75; NA = 89) had salivary cortisol data at the first and 3rd assessments. Because these data points were needed to identify individuals who increased in cortisol across the initial three waves, our final sample consisted of these 164 individuals. Notably, this subsample did not differ from the original sample on focal variables or the sample characteristics including sex or group distribution, age, SES, or parent/child reports on internalizing/externalizing from assessment 1.

Procedures

The current study is the first to report findings from the 4th follow-up assessment. During this assessment, both participants and their parents completed online questionnaires focused on youth‟s mental health, social and emotional adjustment. This assessment took place during the pandemic, from July to September, 2020. Accordingly, pandemic-related stress questions were also included in the questionnaires. Both the original study and the follow-up study were approved by the Institutional Review Board at the University of Minnesota (IRB protocol numbers 1210S21784 and 00009980).

Trier Social Stress Test for Children.

In the first three laboratory assessments, children participated in a modified version of the Trier Social Stress Test for Children (TSST-C; Yim. Quas, Rush, Granger, & Skoluda, 2015), a commonly used laboratory procedure to induce psychological stress and changes in cortisol concentration (Kirschbaum, Pirke, & Hellhammer, 1993). In this social evaluative task, participants give a 5-minute speech, pretending to introduce themselves to an imaginary classroom. Participants were given 5 minutes to prepare for their speech and write notes but could not use the notes during the speech period. The speech was given in a small room with a one-way mirror and visible camera. The experimenter stood behind the mirror, gave instructions through a speaker, and rated the speech for quality and effectiveness. Participants were told that the experimenter was behind the mirror with a teacher who would also be watching and judging their speech. Instructions before the speech were played from a recording of a male‟s voice (the teacher) to ensure that all participants heard the same instructions and perceived someone else was behind the mirror to judge their speech. The recording also told children that they were being videotaped so that other students could rate them, adding to the social-evaluative stress of the task. If participants stopped their speech before five minutes, they were told to “continue” by the experimenter over the speaker. The experimenters remained neutral which increased the uncertainty about one‟s performance. After the speech section, participants performed a verbal arithmetic task aloud for an additional 5 minutes, a standard part of the TSST-C.

Saliva Cortisol Collection.

Saliva Cortisol Collection. Saliva samples were collected seven times during 3 sessions (−20, 0, +5, +20, +40, +60, and +80 min, where 0 represents the beginning of 5-min preparatory period before the TSST-C). See Figure 1 for a depiction of the TSST-C collection timeline. The beginning of speech prep was used as time 0 because previous studies have shown that cortisol production begins to increase in anticipation of the speech rather than due to giving the speech itself (Sumter et al., 2010). Peak salivary cortisol levels are generally reached 20–40 min post stressor onset (Kirschbaum & Hellhammer, 1994), and we have included several samples at 20-min intervals post stressor to capture peak levels as well as decline back to baseline. In order to control for time of day effects that may emerge from diurnal variation in cortisol levels, all sessions began between 3:00 pm and 4:30 pm and ran for 2 hr. The samples were stored in a laboratory freezer at −20°C until being shipped to the University of Trier, Germany. All seven saliva samples were assayed for cortisol concentration in duplicate using a time-resolved fluorescence immunoassay (DELFIA). The intraassay coefficients of variation were between 4.0% and 6.7%, and the corresponding interassay coefficients of variation were between 7.1% and 9.0%. All of the samples from each participant were included in the same assay batch. Biologically implausible cortisol values above 2 μg/dl were removed. Log10 transformations were performed for all cortisol values to resolve positive skew.

Figure 1.

Figure 1.

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TSST session timeline. Saliva samples are indicated by the water droplets beneath the timeline. Saliva samples in the dashed box were included in the AUCi values used in the current study. Adapted with permission from Gunnar et al. (2019)

Youth Self- Report.

At the fourth online follow-up assessment youth completed the MacArthur Health and Behavior Questionnaire (HBQ-C 2.l; Essex et al., 2002) designed to assess physical and mental health symptoms. Youth also completed a questionnaire related to exposure, hardship, and behaviors surrounding Covid-19 (C-19; partially adapted from CRISIS, Nikolaidis et al, 2020), and reported on their state anxiety using the State-Trait Anxiety Inventory-for Children (STAIC; Kirisci, Clark, & Moss, 1997). Finally, youth reported on their emotion regulation strategies via the Emotion Regulation Questionnaire (ERQ; Gross & John, 2003).

Parent Report.

At the fourth follow-up assessment parents again reported on their children‟s physical and mental health via the MacArthur Health and Behavior Questionnaire (HBQ-P 2.1l; Essex et al., 2002). In addition, parents reported on their perception of their child‟s emotionality and regulation via the Emotion Regulation Checklist (ERC; Shields & Cicchetti, 1997).

Measures

Cortisol Reactivity (AUCi).

Area under the curve with respect to increase (AUCi) is a formula used to capture a cortisol change. Specifically, AUCi emphasizes changes over time and is related to the sensitivity of the hormonal system, as the formula accounts for sensitivity and intensity. Thus, the AUCi formula is useful to derive a stress response over an event period (Fekedulegn et al., 2007) and can be thought of as an index of sensitivity of the system in response to a stressor, in this case, the TSST-C (Morris, Rao, Wang, & Garber, 2014). Formulas for the calculation of AUCi are derived from the trapezoid formula, using simple additions of areas of triangles and rectangles (Fekedulegn et al., 2007; Pruessner, Kirschbaum, Meinlschmid, & Hellhammer, 2003). AUCi is calculated from the area under the curve across samples minus the area under the curve below the baseline. In the present study, AUCi was calculated from participants‟ salivary cortisol from the 5-time points relevant to the TSST, using the pre-stress sample as a baseline (see Figure 1 for depiction of the 5 timepoints used in the current study). We chose this measure as it reflects the overall cortisol response to the TSST, and is most consistent with previous manuscripts where we investigated the concurrent and longitudinal associations between cortisol and behavioral functioning (Perry et al., 2020, 2021). To preserve power, any missing samples were imputed as follows: cortisol was taken as the mean of the nearest neighbor samples for a subject, and the modal time across the study for that sample was used. Imputations were only performed if a person was missing a single sample. This resulted in 4 imputations across all three sessions, or 0.01%. Thus, AUCi was included to examine participants‟ cortisol response sensitivity to the speech and math task, with higher scores representing greater cortisol reactivity during the TSST-C.

State Anxiety.

The State subscale of the STACI includes 20 items and is constructed to ask children how they feel at the particular moment in time when filling out the questionnaire. A sample STAIC-State scale question is “I feel very nervous, nervous, not nervous.” Scores ranged from 20–60. The State subscale had good reliability within the current study sample (α = .88).

Youths’ Internalizing Symptoms.

Children‟s internalizing symptoms were assessed from self-report using the Internalizing Scale of the HBQ-C and from parent report using the Internalizing Scale of the HBQ-P. Internalizing was comprised of three subscales: Depression, Separation Anxiety, and Overanxious. The youth-reported internalizing subscale had good internal reliability within our sample (38 items, α = .94). The parent-reported internalizing subscale also had good internal reliability within our sample (42 items, α = .93). A composite of both parent and child-reported internalizing (r = .48, p<.05) was created by averaging the z-scores associated with each measure.

Youths’ Externalizing Symptoms.

Children‟s externalizing symptoms were assessed from parent report using the Externalizing Scale of the HBQ-P. Externalizing was comprised of four subscales: Opposition/Defiance, Conduct Problems, Overt Hostility, and Relational Aggression. Parents selected (0) “never or not true”, (1) “sometimes or somewhat true”, or (2) “often or very true” to each question. The externalizing subscale was created by averaging the appropriate items and had good internal reliability within our sample (38 items, α = .91). Scores ranged from 0–1.20. Youth did not report on their own externalizing behaviors.

Youths’ Emotion Regulation.

Youths‟ emotion regulation was assessed from self-report of the use of cognitive reappraisal strategies ERQ. The cognitive reappraisal subscale is comprised of 6 items rated on a 7-point Likert-type response scale. Higher scores on the scale indicate greater use of the cognitive reappraisal as an adaptive emotion regulation strategy. The cognitive reappraisal subscale was created by taking an average of the appropriate items and had adequate internal consistency (α = .84). Scores ranged from 1–7.

Youths’ Negative Emotional Reactivity.

Parent‟s report of youths‟ negative emotional reactivity was assessed via the negativity/lability subscale of the ERC. The negativity lability subscale includes 15 items rated on a 4-point Likert scale that assess aspects such as angry reactivity and emotional intensity, and includes items such as “exhibits wide mood swings” and “is easily frustrated.” The negativity/lability subscale was created by taking an average of the appropriate items and had adequate internal consistency (α = .87). Scores ranged from 1–3.07.

Youths’ Covid-19 exposure.

The extent to which youth themselves, their friends, or their family members were diagnosed, hospitalized, or died from Covid-19 was assessed via the Covid-19 questionnaire, resulting in a Covid-19 exposure variable.

Data Analytic Plan

Our primary question of interest was whether increases in cortisol across the three assessments during the adolescent period (S1-S3) were associated with poorer mental health and emotional adjustment into late adolescence and early adulthood (S4) for PI youth. Modeling slopes of AUCi values across the three sessions is the ideal analytic strategy. However, the limitation of 3 assessments restricts prediction to a linear slope, which did not fit the pattern of data. This is likely because the AUCi means for PI youth at each session did not demonstrate overall linear change (S1 M = −.001; S2 M = −.014; S3 M = −.007). We then examined the AUCi means within the NA group and the same non-linear pattern emerged (S1 M = −.010; S2 M = −.008; S3 M = −.005), indicating that the non-linear mean change in AUCi values was not unique to the PI sample. Upon examination of the data, it was clear some youth increase in AUCi values across the 3 sessions, referred to as “risers” in the current study, while other youth decrease or stay the same, referred to as “non-risers” in the current study. Given the small cell sizes when broken down by group and pattern of change (PI vs NA and riser vs. non-riser; see Table 1), modeling linear slopes by group and pattern to examine whether individual variation in change over time predicted multiple subsequent outcomes, was not feasible.

Table 1.

Descriptive Statistics of Study Variables by Group and Pattern

Previously-Institutionalized (PI)
  Non-Adopted (NA)
Riser (n=32) Non-riser (n=43) Riser (n=41) Non-Riser (n=48)
Study Variables M SD M SD M SD M SD
Age at Session 4 16.15 1.9 17.05 2.46 16.27 2.13 16.43 2.50
State Anxiety 32.06 5.39 31.73 6.76 32.52 6.89 23.23 6.89
AUCi S1 −.05 .10 .03 .06 −.03 .05 .03 .06
AUCi S2 −.02 .08 −.01 .04 −.01 .05 −.01 .06
AUCi S3 .01 .05 −.03 .03 .03 .05 −.03 .04
Internalizing Behaviors .35 .87 .00 .85 −.20 .82 −.01 .92
Externalizing Behaviors .30 .24 .19 .21 .13 .13 .13 .13
Emotion Regulation 4.16 .88 4.79 1.26 4.54 1.07 4.26 1.38
Negative Emotional Reactivity 1.81 .44 1.56 .33 1.44 .37 1.46 .32
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Instead, we took a conservative approach and created a dichotomous pattern of change variable that identified whether a participant was a riser or a non-riser from S1 to S3 (riser = 1; non-riser =0). Thus, any individual who increased in AUCi from S1 to S3, regardless of magnitude, was labeled a “riser.” Given our use of this crude measure, we felt it was important to categorize youth as riser or non-riser based on change that occurred across the entire 3 years, rather than include participants who only changed across two time points. Next, we verified that the percentage of participants who increased versus stayed the same in S4, this breakdown did not differ from that of the original sample (44% of participants increase in the full sample, 46% of participants increase in the current sample; χ2 (1, N = 214) = .93, p = .34).

Although this analysis cannot identify whether the magnitude of change is associated with later outcomes, we are able to elucidate whether the pattern of change (increasing or not) in cortisol across the peripubertal period is associated with subsequent functioning differently for NA and PI youth. Specifically, we test whether the pattern of change in AUCi (riser vs non-riser) across the peripubertal period is associated with social and emotional adjustment in late adolescence/early adulthood, and whether these effects are different for PI vs NA youth. A path analysis was conducted to test whether the interaction between group and pattern (riser vs. non-riser status) predicted internalizing and externalizing behaviors, as well as emotion regulation and emotional negative reactivity at S4. Mplus (Version 8; Muthén & Muthén, 2017) was used to conduct the analyses and Full Information Maximum Likelihood (FIML) was used to handle missing data. Model fit was assessed by examining the comparative fit index (CFI) (Marsh, Hau, & Grayson 2005), the Tucker-Lewis index (TLI) (Bentler, 1990), the standardized root mean square residual (SRMR), and the root mean square error of approximation (RMSEA) (Cole & Maxwell, 2003). Values close to or greater than .95 indicate good model fit for the CFI and TLI, values less than .06 indicated good model fit for RMSEA, and values less than or equal to .08 indicate good model fit for SRMR (Hu & Bentler, 1999).

Participant age, sex, and state-anxiety were entered in the model as covariates. State anxiety was chosen as a covariate to remove variance associated with how youth were feeling in that particular moment and instead allow for a greater focus on the extent to which they usually experienced internalizing symptoms in their day-to-day functioning. Although Covid-19 questions are not the focus of the current investigation, the Covid-19 pandemic was taking place during data collection. Thus, the covid-19 exposure variable was also tested as a covariate in the model. However, it was not associated with any of the primary study variables and therefore its inclusion weakened model fit. Duration of time spent in institutional care was also tested as a covariate but its inclusion did not change structural pathways and weakened model fit. Thus, we removed duration of institutional care and the covid-19 exposure variables from the model, and trimmed non-significant pathways for parsimony.

Results

Descriptive statistics and correlations for study variables by group are presented in Tables 1 and 2. For both NA and PI youth, significant correlations emerged among the mental health and emotional adjustment variables, though stronger correlations among these variables were evident for the PI youth. Importantly, the pattern variable (riser vs. non-riser) was significantly associated with each adjustment outcome for PI youth but not for NA youth, providing preliminary insight into the proposed moderation effect.

Table 2.

Correlations among Model Variable by Group

PI Youth 1 2 3 4 5 6 7
1. Age --
2. Sex −.01 --
3. Pattern (riser vs. non-riser) −.19 −.07 --
4. Internalizing −.08 .28* .21* --
5. Externalizing −.28* −.16 .23* .21* --
6. Emotion Regulation .17 −.11 −.27* −.48** -.25* --
7. Emotional Reactivity −.28* −.15* .31** .33** .78** −.37** --
8. State Anxiety .14 .07 .03 .46** .05 .37** .05
NA Youth 1 2 3 4 5 6 7
1. Age --
2. Sex −.10 --
3. Pattern (riser vs. non-riser) −.03 −.05 --
4. Internalizing .03 .12 −.11 --
5. Externalizing −.11 −.09 .00 .43** --
6. Emotion Regulation .11 −.11 .11 −.31** .04 --
7. Emotional Reactivity −.12 .04 −.03 .48** .75** −.03 --
8. State Anxiety .09 .21* .02 .60* .19 −.48* .27*
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Note:

*

p < .05

**

p < .001; riser = 1, non-riser =0; male = 1 female = 2.

The overall model testing our primary question of interest was a good fit to the data, χ2(4, N = 164) = 5.50 p = .24, CFI = .99, TLI = .96, SRMR = .03, RMSEA = .05 [CI = .00, .09] (standardized coefficients are presented in Figure 2). Examination of covariate effects revealed that child age was associated negatively with externalizing behaviors (β = −.18 (.07), p = .01) and negative emotional reactivity (β = −.16 (.07), p = .02), indicating that older youth were less likely to engage in externalizing behaviors and showed less negative emotional reactivity. Child sex was associated positively with youths‟ internalizing behaviors (β = .13 (.08), p =.01) indicating that girls were more likely to show internalizing behaviors than boys.

Figure 2. Standardized Model Estimates.

Figure 2.

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Note: Only significant pathways are depicted. Risers are coded 1 and non-risers are coded 0; NA youth are coded 1 and PI youth are coded 2; * p <.05, + *p <.10.

Evidence that increases in cortisol across the peripubertal period are associated with poorer mental health and social and emotional functioning into late adolescence and early adulthood also emerged (see Figure 2). Specifically, the group by pattern interaction significantly predicted internalizing behaviors (β = .21 (.23), p = .04), emotion regulation abilities (β = −.28(.24), p =.02), and negative emotional reactivity (β = .25 (.23), p =.03) at S4. Of note, there was also a trend level association between the group by pattern interaction and externalizing behaviors (β = .20 (.23), p = .08). Because the group and pattern variables were both dichotomous, adjusted means were plotted and mean differences were examined for each outcome variable to visualize significant interactions and simple effects (see Figure 3).

Figure 3. Plotted Estimated Marginal Means by Group and Pattern.

Figure 3.

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Note: Mean differences were examined to test for simple effects. NS = not significant, * = p <.05, ** = p < .01. Internalizing symptoms reflect a z-scored composite of parent and youth report. Externalizing symptoms, emotion regulation, and emotional reactivity were all created by averaging the appropriate items on the original scales.

Discussion

Findings from the current study demonstrate that PI youth who increased in cortisol reactivity (AUCi) across the 3 assessments during the peripubertal period were significantly more likely to have greater internalizing problems, be poorer at regulating their emotions, and display greater negative emotional reactivity than NA youth, years after initial cortisol increases. Thus, we found no evidence that social, emotional, or behavioral symptoms improve over time for youth who show increases in cortisol reactivity across childhood and adolescence. Rather, increases in cortisol reactivity across late childhood and adolescence may be associated with greater psychopathology, particularly anxiety and depression, and poorer social functioning well into late adolescence and early adulthood.

Currently, we know relatively little about social and emotional functioning in teens and young adults who experienced early institutional care. However, findings fit with previous work demonstrating that internalizing symptoms and social difficulties can persist or increase in mid-adolescence and very early adulthood for PI youth (Hawk & McCall, 2010; Humphreys et al., 2015; Sonuga-Barke, Schlotz, & Kreppner, 2010). For example, Sonuga-Barke and colleagues showed that PI children who experienced at least 6 months of institutional care began to display increases in emotional problems during mid-adolescence (Sonuga-Barke, Schlotz, & Kreppner, 2010), and further increases between early adolescence and young adulthood relative to children who experienced little to no deprivation (Sonuga-Barke et al., 2017). If at the cusp of adulthood, PI youth continue to have greater difficulty managing emotions and behavior, this could forecast increased challenges when forming relationships and pursuing career opportunities. Moreover, socioemotional deficits during the transition to adulthood could signal continued mental health symptoms that may lead to psychopathological diagnosis if left untreated. What remains unclear is whether the behavioral and emotional deficits are side effects of the biological disruption, or if they trigger an underlying diathesis to mental health difficulties.

One plausible mechanism underlying the link between cortisol reactivity and socioemotional deficits relates to alterations in brain structure that developed in response to early life adversity. What was once functional in a deprived environment might no longer be effective following recalibration in an enriched environment. There is a U shape relation between glucocorticoids (i.e. cortisol) and behavioral functioning (Herbert et al., 2006) that suggests under activity or over activity of the HPA axis during times of stress would be associated with suboptimal outcomes. What counts as under and over activity, however, may depend on activity of the axis during the development of neural systems involved in threat and emotion processing. In the context of institutional care, the HPA axis appears to down-regulate, producing lower levels of cortisol and blunted cortisol responses to stressors (DePasquale et al., 2019; McLaughlin et al., 2015). There is evidence, though, that even in the context of hypocortisolism the amygdala becomes more reactive to threatening stimuli and is less well-regulated by medial prefrontal circuitry (vanTiegham and Tottenham, 2018). These emotion-regulatory circuits may respond to the recalibration of the HPA axis during the peripubertal period with heightened sensitivity. If so, PI youth may experience psychological stress more intensely as a result of increased cortisol reactivity, making it more difficult to manage emotions and behavior, or employ coping mechanisms that tend to be more successful in situations of lower intensity. In line with these hypotheses, there is growing evidence linking too much cortisol, or hypercortisolism, to greater internalizing behavior problems (see Strüber, Strüber, & Roth, 2014 for a review). If PI individuals are not psychologically or biologically able to manage the increased cortisol, even if cortisol levels are normative to NA peers, similar findings would be expected. Although possible, this hypothesis is difficult to directly test in humans and we lack rodent models where such testing could be conducted, as hypocortisolism does not appear to be the pattern associated with early deprivation in rodents.

Although previous work with this sample was optimistic about the plasticity in HPA functioning and recalibration across the pubertal period (Gunnar et al., 2019), the results presented in the current study, as well other subsequent work from this sample (Perry et al., 2020; Perry et al., 2021), suggest that identifying PI youth who recalibrate as „recovered‟ may be too simplistic of a view. The work presented here is preliminary and additional research needs to be conducted to better understand the complicated pattern of recovery following the early deprivation of institutional rearing. Recalibration of the HPA axis during the open pubertal window may in fact be positive; a functioning stress response system is likely to support the body during challenge. However, it might not be the case that recovery in one system leads to recovery across all domains, and recovery across domains may not happen at the same pace. It is also possible that recovery in HPA axis functioning is associated with downstream processes that are not yet known, or underlie additional challenges for PI youth. In the current study, we were not able to model recalibration and instead relied on a crude dichotomous split between „risers‟ and „non-risers.” Thus, we are careful not to make broad claims regarding the functional outcomes of recalibrated HPA systems on these data alone. Instead, we believe this is a first step toward hypothesis generation for future work aiming to elucidate the complex associations between HPA functioning and adjustment following early institutional care. For example, we were not able to test whether the magnitude of change in cortisol reactivity over time was associated with increased mental health symptoms. Future research, with larger samples, is needed to identify whether the extent to which cortisol increases over time for PI youth is an indicator of future socioemotional functioning, or whether recalibrating at all is most predictive.

It will be important for researchers to continue to follow PI individuals as they navigate the challenges of early adulthood such as attending higher education, entering the workforce, and even potentially becoming parents themselves. These life stages require significant emotional and behavioral control and social adaptation. Individuals who demonstrate poorer social and emotional competencies struggle to complete their education (Taylor, Oberle, Durlak, Weissberg, 2017), advance in their careers (Heimler, Rosenberg, & Morote, 2012), and parent their own children in sensitive and responsive ways (Morelen, Shaffer, & Suveg, 2016). Thus, continued social and emotional problems is one potential mechanism that may link deprivation in infancy to adulthood maladjustment.

Although the current study provides valuable insight, it is not without limitations. First, although cortisol increases across adolescence were associated with later social and emotional deficits for PI youth, only 14% of PI youth were considered to be above the clinical threshold of 3.55 for youth-reported internalizing symptoms (Wiik et al., 2010). In addition, only 22% of PI youth were above the clinical threshold of .72 for parent-reported internalizing symptoms (Lemery-Chalfant et al., 2007). Thus, the clinical relevance of our findings is yet to be determined. It is important to note, however, that 5% of PI youth-reported, and 7% of PI parent-reported, internalizing behaviors reached clinically significant levels at assessment 3. Thus, from assessment 3 to assessment 4, these percentages substantially increased. Future research is needed to determine if internalizing symptomatology continues to escalate throughout the adult years.

A second limitation of the current study is that we did not consider aspects of the current social environment that may weaken the association between cortisol increases and socioemotional deficits. For example, highly sensitive parents who provide young people with the tools for managing intense emotions, or peer groups and friendships who provide a context of great support, may weaken these associations. Future research is needed to better understand the role of changing social environments as young people move into adulthood. Predicting resilience is as important as predicting negative outcomes.

Additionally, we examined AUCi and not the area under the curve from ground. Recalibration of the HPA axis appears to involve both an increase in levels and reactivity (see Gunnar et al., 2019). Thus, in this paper we only focused on one dimension of recalibration, as this dimension of reactivity is most critical to an analysis of stress reactivity. Whether overall increases in basal levels is also involved in challenging regulation of emotion circuits remains to be determined, perhaps with data on diurnal cortisol activity.

Finally, data from the current study were collected during the covid-19 pandemic and although we tested whether specific measures of pandemic stress were associated with our outcomes of interest, other unmeasured aspects of the pandemic may contribute to the current findings, especially the increase in anxiety and depression. However, the vastly different pattern in associations between PI and NA youth, who both experienced pandemic related stress, provide some confidence that findings are not merely a stronger reaction to this environmental stressor.

Even with these limitations, the current study adds considerably to the literature on PI youth‟s social and emotional functioning into early adulthood, and elucidates how increases in cortisol reactivity across adolescence may be associated with continued deficits in socioemotional development. Specifically, we were able to show distinct differences in the association between cortisol increases and outcomes for NA and PI youth, with PI youth who show increases in cortisol across adolescence consistently experiencing subsequent negative outcomes. The initial optimism of HPA recalibration may be tempered by a complicated pathway toward recovery from early deprivation. This work underscores the importance of investigating potential causal mechanisms that help explain these associations and continuing to assess PI youth into adulthood to gain a clearer understanding of the clinical implications and long-term consequences of early life stress.

Highlights:

  • PI Stress recalibration linked to later socioemotional maladjustment

  • Cortisol increases across puberty linked to internalizing behaviors for PI youth

  • Cortisol increases across puberty linked to emotional dysregulation for PI youth

  • Cortisol increases across puberty linked to emotional reactivity for PI youth

  • No associations for NA youth

Acknowledgments:

The authors wish to thank the families who devoted many hours to the longitudinal study from which the current data were taken. Special thanks to Bao Moua, Teresa Grunklee, & Abby Cavanaugh who helped recruit, collect, and process the data. This research was supported by a grant from the National Institute of Child Health and Human Development through the National Institutes of Health [5R01 HD075349] to the final author. The authors have declared that they have no competing or potential conflicts of interest. Carrie DePasquale passed away in September of 2020 after designing and helping to start this study.

Footnotes

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Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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