Elsevier

Psychoneuroendocrinology

Volume 67, May 2016, Pages 18-26
Psychoneuroendocrinology

Differential sensitization of parenting on early adolescent cortisol: Moderation by profiles of maternal stress

https://doi.org/10.1016/j.psyneuen.2016.01.025Get rights and content

Highlights

  • Profile analytic approach to examine how phenotypes of maternal stress co-occur.

  • Mothers with concurrent parenting and childhood stress appear to be most at-risk.

  • The effects of parenting on child diurnal cortisol slope depend on maternal stress.

  • One-size-fits-all approach to parent training interventions may need re-evaluation.

Abstract

The hypothalamic–pituitary–adrenal (HPA) axis is a critical component of the body’s stress-response neurobiological system, and its development and functioning are shaped by the social environment. Much of our understanding of the effects of the caregiving environment on the HPA axis is based on (a) parenting in young children and (b) individual maternal stressors, such as depression. Yet, less is known about how parenting behaviors and maternal stressors interact to influence child cortisol regulation, particularly in older children. With an ethnically diverse sample of 199 mothers and their early adolescent children (M = 11.00 years; 54% female), a profile analytic approach was used to investigate how multiple phenotypes of maternal stress co-occur and moderate the relation between parenting behaviors and youths’ diurnal cortisol rhythms. Latent profile analysis yielded 4 profiles: current parenting stress, concurrent parenting and childhood stress, childhood stress, and low stress. For mothers with the concurrent parenting and childhood stress profile, inconsistent discipline, poor parental supervision, and harsh caregiving behaviors each were related to flattened diurnal cortisol rhythms in their adolescents. For mothers with the current parenting stress and childhood stress profiles, their use of inconsistent discipline was associated with flattened diurnal cortisol rhythms in their adolescents. For mothers with the low stress profile, none of the parenting behaviors was related to their adolescents’ cortisol regulation. Findings suggest that based on mothers’ stress profile, parenting behaviors are differentially related to youths’ diurnal cortisol rhythms. Implications for parenting interventions are discussed.

Introduction

The hypothalamic–pituitary–adrenal (HPA) axis is a critical component of the stress-response neurobiological system that responds to physical and psychological stressors via a cascade of neuroendocrine hormones, ending with cortisol. Although genetic and prenatal programing effects are linked to neurobiological development and functioning (Bartels et al., 2003, Belsky and Pluess, 2009), the development of the HPA axis is also shaped by environmental experiences (Del Giudice et al., 2011); this is especially true of early caregiving experiences, as evidenced in both nonhuman primates (Sánchez, 2006) and children (Hostinar et al., 2014, McEwen, 2012). Considerable work in this area has centered around infants and young children, thus, much of our understanding of how parenting practices influence the developing HPA axis is based on sensitive, responsive, and consistent parenting (Hostinar et al., 2014), the fundamental caregiving behaviors for infants and young children (Ainsworth et al., 1974). However, little is known about the effects of parenting practices on the HPA axis in early adolescence, a developmental period associated with heightened stress and emotional responsiveness to the social environment (Steinberg and Morris, 2001), as well as increased conflict with parents (Marceau et al., 2015). Accumulating evidence suggests that the HPA axis becomes more reactive to stress during adolescence (Gunnar et al., 2009, Klein and Romeo, 2013, Lupien et al., 2009). Thus, a better understanding of how key parenting behaviors are related to HPA functioning in early adolescence is needed and may have important clinical implications for designing effective parenting interventions aimed at improving stress reactivity and regulation.

Extensive research has identified inconsistent discipline, poor parental supervision, and harsh parenting as salient parenting behaviors linked to adolescents’ poor emotion regulation, externalizing behavior problems, and substance use (Duncombe et al., 2012, Luyckx et al., 2011, MacKenzie et al., 2013). Albeit limited, evidence suggests that as with neglectful early care (Bruce et al., 2009, Johnson et al., 2011), poor parental supervision (Martin et al., 2014) has been linked to flatter slope in morning-to-evening cortisol in older children. In contrast, inconsistent discipline and harsh parenting have not been found to affect diurnal cortisol rhythms in early adolescence (Martin et al., 2012, Martin et al., 2014). It may be that in comparison to inconsistent discipline and harsh parenting, parental supervision is a better predictor of cortisol regulation in older children. Alternatively, because parenting does not occur in isolation, parents’ experiences of stress may differentially affect the influence of parenting behaviors on HPA axis functioning.

Numerous studies have linked environmental stressors, particularly in mothers, to their children’s dysregulated HPA functioning. Parental stress (Fisher and Stoolmiller, 2008, Koch et al., 2010), interparental aggression (Sturge-Apple et al., 2012), parental substance use while controlling for the number of adverse life events experienced by their children (Evans et al., 2013), maternal depression (Lupien et al., 2000), and socioeconomic disadvantage (Lupien et al., 2000, Zalewski et al., 2012) have all been associated with dysregulated child cortisol. Experiences of childhood abuse have likewise been associated with dampened cortisol reactivity in adulthood (Carpenter et al., 2007). In contract, less is known about how maternal childhood abuse impacts her child’s cortisol regulation. This body of research highlights the link between maternal stress and youths’ cortisol reactivity and regulation, yet the manner in which such stressors influence the relationship between parenting behaviors and child cortisol is not well understood. Moreover, a limitation of the aforementioned research is that most studies examined individual stressors in isolation (Sturge-Apple et al., 2012) or combined the stressors into a composite (Martin et al., 2012) or cumulative risk index (Zalewski et al., 2012). These methods lack specificity, as such stressors often co-occur in meaningful ways. A more ecologically valid way to examine the effects of maternal stress involves assessing multiple indicators of stress to determine distinct patterns of co-occurrence, in tandem with examining the more proximal role of parenting behaviors.

Our study used a latent profile analytic approach to investigate how phenotypes of maternal stress moderate the relationship between inconsistent discipline, poor parental supervision, and harsh parenting behaviors and early adolescent diurnal cortisol rhythms in 9–12-year-olds (Fig. 1). We examined multiple indicators of mothers’ current as well as childhood stress due to exposure to child abuse. Based on findings that childhood abuse history alone may be insufficient but when combined with ongoing stress in the form of depression or other psychological stressors, is related to neurobiological dysregulation (Heim et al., 2004, Kaufman et al., 1997, Rinne et al., 2002), we expected at least 4 groups with distinctive stress profiles: a low stress group, a group with current high levels of stress, a group with high levels of childhood but not current stress, and a group with high levels of current and childhood stress. Further, based on prior findings on the association between parenting behaviors and diurnal cortisol rhythms in early adolescence (e.g., Martin et al., 2014) we hypothesized that there would be a direct link between parenting behaviors and diurnal cortisol rhythms in early adolescence. We further hypothesized that the associations between parenting behaviors and youths’ diurnal cortisol rhythms would be stronger in the presence of maternal stress, particularly for combined childhood and current stress (e.g., Heim et al., 2004).

Section snippets

Participants

The present data were collected as part of a follow-up assessment from youths and families who had participated in the Healthy Families America (HFA) San Diego clinical trial from child birth to age 3 (Landsverk et al., 2002). For detailed information about the original study and sample see Martin et al. (2014). For our study, a total of 239 families, of the original 488, were recruited. Families were excluded if the participating caregiver was not the youth’s biological mother (n = 33), if the

Latent profile analysis of maternal stress

Table 2 shows the model fit statistics from step 1 of the 3-step LPA from models with 2–5 profiles. Although the BLRT indicated that each model had a significantly better fit than did the prior model, the information criteria indicators, in general, indicated that the 4-profile model had the best fit. Additionally, the fit indices of the 5-profile model increased from those of the 4-profile model, which had the lowest values. Entropy was also the highest for the 4-profile model and in the

Discussion

The purpose of the present study was to examine whether the association between parenting behaviors and youth’s HPA axis functioning would vary depending on parental stress in early adolescence. The findings indicated that when multiple potential stressors are considered, the mothers in this study experienced distinctive patterns of stress, with three stress profiles – current parenting stress, concurrent parenting and childhood stress, and childhood stress – and one low stress profile.

Conclusions

Despite its limitations, our study contributes to the literature in numerous ways. Our study supports a model of differential sensitization of the HPA axis based upon maternal parenting practices. The relationship of the specific parenting behaviors examined – inconsistent discipline, parental supervision, and harsh parenting – with adolescent diurnal cortisol profiles depended on mothers’ experience of current and ongoing stress. This finding suggests that the widely accepted one-size-fits-all

Conflict of interest

The authors have no conflicts of interest to disclose.

Role of funding source

Funding for this study was provided by the following grants: HD045894, NICHD, U.S. PHS; MH059780 and MH078105, NIMH, U.S. PHS; and DA023920, NIDA, U.S. PHS. The funding organizations had no further role in the study design; in the collection, analysis, and interpretation of the data; in the writing of this paper; or in the decision to submit the paper for publication.

Contributors

Phil Fisher designed the original study and wrote the protocol. All of the authors made contributions to the conceptualization of the study. Christina Gamache Martin conducted the literature review and statistical analyses. Hyoun Kim assisted in and reviewed the analyses. Christina Gamache Martin wrote the first draft of the manuscript. All authors contributed to and approved of the final manuscript.

Acknowledgements

Funding for this research was provided by the following grants: HD045894, NICHD, NIH, U.S. PHS; MH059780, and MH078105, NIMH, NIH, U.S. PHS; and DA023920, NIDA, NIH, U.S. PHS. The authors thank the families who participated in the study; John Landsverk, Cynthia Connelly, and their colleagues at the Child and Adolescent Services Research Center in San Diego, and Cheryl Mikkola for editorial assistance.

References (65)

  • Z.A. Klein et al.

    Changes in hypothalamic–pituitary–adrenal stress responsiveness before and after puberty in rats

    Horm. Behav.

    (2013)
  • K.J. Koss et al.

    Social deprivation and the HPA axis in early development

    Psychoneuroendocrinology

    (2014)
  • M.G. Kroupina et al.

    Adoption as an intervention for institutionally reared children: HPA functioning and developmental status

    Infant Behav. Dev.

    (2012)
  • S.J. Lupien et al.

    Child’s stress hormone levels correlate with mother’s socioeconomic status and depressive state

    Biol. Psychiatry

    (2000)
  • B.L. Mah et al.

    Oxytocin in postnatally depressed mothers: its influence on mood and expressed emotion

    Prog. Neuropsychopharmacol. Biol. Psychiatry

    (2013)
  • C.G. Martin et al.

    Child diurnal cortisol rhythms parenting quality, and externalizing behaviors in preadolescence

    Psychoneuroendocrinology

    (2014)
  • C.G. Martin et al.

    Racial and ethnic differences in diurnal cortisol rhythms in preadolescents: the role of parental psychosocial risk and monitoring

    Horm. Behav.

    (2012)
  • P.S. Nurius et al.

    Life course pathways of adverse childhood experiences toward adult psychological well-being: a stress process analysis

    Child Abuse Negl.

    (2015)
  • T. Rinne et al.

    Hyperresponsiveness of hypothalamic–pituitary–adrenal axis to combined dexamethasone/corticotropin-releasing hormone challenge in female borderline personality disorder subjects with a history of sustained childhood abuse

    Biol. Psychiatry

    (2002)
  • S.J. Russ et al.

    Cortisol levels in response to starting school in children at increased risk for social phobia

    Psychoneuroendocrinology

    (2012)
  • M.M. Sánchez

    The impact of early adverse care on HPA axis development: nonhuman primate models

    Horm. Behav.

    (2006)
  • M.A. Straus et al.

    Identification of child maltreatment with the parent–child conflict tactics scales: development and psychometric data for a national sample of American parents

    Child Abuse Negl.

    (1998)
  • H. Turner et al.

    Stress processes across the life course: introduction and overview

    Adv. Life Course Res.

    (2008)
  • M.D.S. Ainsworth et al.

    Infant-mother attachment and social development: socialisation as a product of reciprocal responsiveness to signals

  • Asparouhov, T., Muthén, B.O., 2014. Auxiliary variables in mixture modeling: 3-step approaches using Mplus (Mplus Web...
  • J. Belsky et al.

    The nature (and nurture) of plasticity in early human development

    Perspect. Psychol. Sci.

    (2009)
  • J. Bruce et al.

    Morning cortisol levels in preschool-aged foster children: differential effects of maltreatment type

    Dev. Psychobiol.

    (2009)
  • Capaldi, D.M., 1995. Discipline Questionnaire. Eugene, OR: Oregon Social Learning Center. Unpublished...
  • Capaldi, D.M., Wilson, J., 1998. Monitor and Parent–Child Relationship Questionnaire. Eugene, OR : Oregon Social...
  • P. Chamberlain et al.

    Parent observation and report of child symptoms

    Behav. Assess.

    (1987)
  • S.S. Dickerson et al.

    Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research

    Psychol. Bull.

    (2004)
  • T. Dix

    The affective organization of parenting: adaptive and maladaptive processes

    Psychol. Bull.

    (1991)
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