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Sex-specific differences in adrenocortical attunement in mothers with a history of childhood abuse and their 5-month-old boys and girls

  • Psychiatry and Preclinical Psychiatric Studies - Original Article
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Abstract

Recent evidence points to the existence of a neurobiological attunement between mother and child, e.g., associations between maternal and child hypothalamic–pituitary–adrenal (HPA) axis functioning. As maternal history of abuse (HoA) has been shown to negatively affect mother–child interaction and HPA-axis functioning, we theorized those experiences to exert an influence on cortisol attunement, and we examined the role of infant gender in this context. Shortly after birth of their first child, a community sample of women was screened using the Childhood Trauma Questionnaire. Mothers reporting moderate or severe sexual and/or physical abuse were included in the maltreatment group (n = 41; MG) and compared with a non-maltreated comparison group (n = 47; CG). At the child’s age of 5 months, mother and infant baseline salivary cortisol was collected on two consecutive days between 11 and 1 o’clock. Correlation analyses confirmed an association between maternal and infant salivary cortisol levels for the complete sample. However, hierarchical regression models revealed a moderating role of maternal HoA and infant gender: in the CG, cortisol attunement was only significant in mother–daughter dyads, whereas in the MG, we found cortisol levels to be associated only in mother–son dyads. Consequently, alterations of neurobiological attunement between mother and child might compose a mechanism for the transgenerational transmission of adverse childhood experiences.

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References

  • Aiken LS, West SG, Reno RR (1991) Multiple regression: Testing and interpreting interactions. Sage Publications, Newbury Park, Calif

    Google Scholar 

  • Atkinson L, Gonzalez A, Kashy DA, Santo Basile V, Masellis M, Pereira J, Levitan R (2013) Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology 38(12):2943–2951

    Article  CAS  PubMed  Google Scholar 

  • Beebe B, Jaffe J, Markese S, Buck K, Chen H, Cohen P, Feldstein S (2010) The origins of 12-month attachment: a microanalysis of 4-month mother–infant interaction. Attach Human Dev 12(1–2):3–141

    Article  Google Scholar 

  • Belsky J, Jaffee S (2006) The multiple determinants of parenting. Dev Psychopathol Risk Disord Adapt 3:38

    Google Scholar 

  • Bernard K, Butzin-Dozier Z, Rittenhouse J, Dozier M (2010) Cortisol production patterns in young children living with birth parents vs children placed in foster care following involvement of child protective services. Arch Pediatr Adolesc Med 164(5):438–443

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernard K, Zwerling J, Dozier M (2015) Effects of early adversity on young children’s diurnal cortisol rhythms and externalizing behavior. Dev psychobiol 57(8):935–947

    Article  CAS  PubMed  Google Scholar 

  • Bernstein DP, Fink LF (1999) Childhood trauma questionnaire (CTQ). Psychol Corp, San Antonio

    Google Scholar 

  • Bernstein DP, Stein JA, Newcomb MD, Walker E, Pogge D, Ahluvalia T et al (2003) Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse Negl 27(2):169–190

    Article  PubMed  Google Scholar 

  • Bert SC, Guner BM, Lanzi RG (2009) The influence of maternal history of abuse on parenting knowledge and behavior. Fam Relat 58(2):176–187

    Article  PubMed  PubMed Central  Google Scholar 

  • Bock J, Poeschel J, Schindler J, Börner F, Shachar-Dadon A, Ferdman N, Gaisler-Salomon I, Leshem M, Braun K, Poeggel G (2014). Transgenerational sex-specific impact of preconception stress on the development of dendritic spines and dendritic length in the medial prefrontal cortex. Brain Struct Funct 219(1):1–9

    Article  Google Scholar 

  • Bornstein MH (2013) Mother–infant attunement: a multilevel approach via body, brain, and behavior. The infant mind: origins of the social brain, 266–298

  • Brazelton TB, Koslowski B, Main M, Lewis M, Rosenblum M, Leonard A (1974) The effect of the infant on its caregiver. In: Lewis M, Rosenblum M (eds) The effect of the infant on its caregiver. Wiley-Interscience, Oxford, England, xxiv, 264

  • Bright MA, Granger DA, Frick JE (2012) Do infants show a cortisol awakening response? Dev Psychobiol 54(7):736–743

    Article  CAS  PubMed  Google Scholar 

  • Castral TC, Warnock F, Dos Santos CB, Daré MF, Moreira AC, Antonini SRR, Scochi CGS (2015) Maternal mood and concordant maternal and infant salivary cortisol during heel lance while in kangaroo care. Eur J Pain 19(3):429–438

    Article  CAS  PubMed  Google Scholar 

  • Criss MM, Shaw DS, Ingoldsby EM (2003) Mother–son positive synchrony in middle childhood: relation to antisocial behavior. Soc Dev 12(3):379–400

    Article  Google Scholar 

  • Derogatis LR, Unger R (2010) Symptom checklist-90-revised. In: Weiner IB, Craighead WE (eds) The Corsini Encyclopedia of Psychology. Wiley, Hoboken, NJ, pp 1743–1744

    Google Scholar 

  • Dixon L, Hamilton-Giachritsis C, Browne K (2005) Attributions and behaviours of parents abused as children: a mediational analysis of the intergenerational continuity of child maltreatment (Part II). J Child Psychol Psychiatry 46(1):58–68

    Article  PubMed  Google Scholar 

  • Driessen M, Herrmann J, Stahl K, Zwaan M, Meier S, Hill A, Osterheider M, Petersen D (2000) Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Arch Gen psychiatry 57(12):1115–1122

    Article  CAS  PubMed  Google Scholar 

  • Easterbrooks M, Biringen Z (2005) The Emotional Availability Scales: Methodological refinements of the construct and clinical implications related to gender and at-risk interactions. Infant Ment Health J 26(4):291–294

    Article  Google Scholar 

  • Egeland B, Jacobvitz D, Sroufe LA (1988) Breaking the cycle of abuse. Child Dev 59(4):1080–1088

    Article  CAS  PubMed  Google Scholar 

  • Else-Quest NM, Hyde JS, Goldsmith HH, Van Hulle CA (2006) Gender differences in temperament: a meta-analysis. Psychol Bull 132(1):33

    Article  PubMed  Google Scholar 

  • Feldman R (2003) Infant–mother and infant–father synchrony: the coregulation of positive arousal. Infant Mental Health J 24(1):1–23

    Article  Google Scholar 

  • Feldman R (2007) Parent–infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. J Child Psychol Psychiatry 48(3–4):329–354

    Article  PubMed  Google Scholar 

  • Feldman R (2012) Parent–infant synchrony: a biobehavioral model of mutual influences in the formation of affiliative bonds. Monogr Soc Res Child Dev 77(2):42–51

    Article  Google Scholar 

  • Feldman R, Granat A, Pariente C, Kanety H, Kuint J, Gilboa-Schechtman E (2009) Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. J Am Acad Child Adolesc Psychiatry 48(9):919–927

    Article  PubMed  Google Scholar 

  • Feldman R, Singer M, Zagoory O (2010) Touch attenuates infants’ physiological reactivity to stress. Dev Sci 13(2):271–278

    Article  PubMed  Google Scholar 

  • Feldman R, Vengrober A, Eidelman-Rothman M, Zagoory-Sharon O (2013) Stress reactivity in war-exposed young children with and without posttraumatic stress disorder: relations to maternal stress hormones, parenting, and child emotionality and regulation. Dev Psychopathol 25(4pt1):943–955

    Article  PubMed  Google Scholar 

  • Franke GH, Derogatis LR (2002) SCL-90-R: symptom-Checkliste von LR Derogatis: deutsche version: manual. Beltz Test

  • Fuchs A, Möhler E, Resch F, Kaess M (2015) Impact of a maternal history of childhood abuse on the development of mother–infant interaction during the first year of life. Child Abuse Negl 48:179–189

    Article  PubMed  Google Scholar 

  • Gartstein MA, Rothbart MK (2003) Studying infant temperament via the revised infant behavior questionnaire. Infant Behav Dev 26(1):64–86

    Article  Google Scholar 

  • Gitau R, Cameron A, Fisk NM, Glover V (1998) Fetal exposure to maternal cortisol. Lancet 352(9129):707–708

    Article  CAS  PubMed  Google Scholar 

  • Gitau R, Fisk NM, Glover V (2004) Human fetal and maternal corticotrophin releasing hormone responses to acute stress. Archiv Dis Child Fetal Neonatal Ed 89(1):F29–F32

    Article  CAS  Google Scholar 

  • Granger DA (1998) Children’s salivary cortisol, internalising behaviour problems, and family environment: results from the Concordia longitudinal risk project. Int J Behav Dev 22(4):707–728

    Article  Google Scholar 

  • Hatzinger M, Brand S, Perren S, von Wyl A, von Klitzing K, Holsboer-Trachsler E (2007) Hypothalamic–pituitary–adrenocortical (HPA) activity in kindergarten children: importance of gender and associations with behavioral/emotional difficulties. J Psychiatr Res 41(10):861–870

    Article  PubMed  Google Scholar 

  • Hayes AF (2012) PROCESS: a versatile computational tool for observed variable mediation, moderation, and conditional process modeling. http://is.muni.cz/el/1423/podzim2014/PSY704/50497615/hayes_2012_navod_process.pdf

  • Hibel LC, Granger DA, Blair C, Finegood ED (2015) Maternal-child adrenocortical attunement in early childhood: continuity and change. Dev Psychobiol 57(1):83–95

    Article  PubMed  Google Scholar 

  • Hostinar CE, Gunnar MR (2013) Future directions in the study of social relationships as regulators of the HPA axis across development. J Clin Child Adolesc Psychol 42(4):564–575

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH (1999) Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus–pituitary–adrenal axis. Psychosom Med 61(2):154–162

    Article  CAS  PubMed  Google Scholar 

  • Klinitzke G, Romppel M, Häuser W, Brähler E, Glaesmer H (2012) Die deutsche Version des Childhood Trauma Questionnaire (CTQ)–psychometrische Eigenschaften in einer bevölkerungsrepräsentativen Stichprobe [The German Version of the Childhood Trauma Questionnaire (CTQ): psychometric characteristics in a representative sample of the general population]. Psychother Psychosom Med Psychol 62(2):47–51

    Article  PubMed  Google Scholar 

  • Kochanska G, Kim S (2014) A complex interplay among the parent–child relationship, effortful control, and internalized, rule-compatible conduct in young children: evidence from two studies. Dev Psychol 50(1):8

    Article  PubMed  Google Scholar 

  • Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C (2004) HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender. Psychoneuroendocrinology 29(1):83–98

    Article  CAS  PubMed  Google Scholar 

  • LeMoult J, Chen MC, Foland-Ross LC, Burley HW, Gotlib IH (2015) Concordance of mother–daughter diurnal cortisol production: understanding the intergenerational transmission of risk for depression. Biol Psychol 108:98–104

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyons-Ruth K, Block D (1996) The disturbed caregiving system: relations among childhood trauma, maternal caregiving, and infant affect and attachment. Infant Ment Health J 17(3):257–275

    Article  Google Scholar 

  • Middlemiss W, Granger DA, Goldberg WA, Nathans L (2012) Asynchrony of mother–infant hypothalamic–pituitary–adrenal axis activity following extinction of infant crying responses induced during the transition to sleep. Early Human Dev 88(4):227–232

    Article  CAS  Google Scholar 

  • Moehler E, Biringen Z, Poustka L (2007) Emotional availability in a sample of mothers with a history of abuse. Am J Orthopsychiatry 77(4):624

    Article  PubMed  Google Scholar 

  • Neu M, Laudenslager ML, Robinson J (2008) Coregulation in salivary cortisol during maternal holding of premature infants. Biol Res Nurs 10(3):226–240

    Article  PubMed  Google Scholar 

  • Nicol-Harper R, Harvey AG, Stein A (2007) Interactions between mothers and infants: impact of maternal anxiety. Infant Behav Dev 30(1):161–167

    Article  PubMed  PubMed Central  Google Scholar 

  • Papp LM, Pendry P, Adam EK (2009) Mother-adolescent physiological synchrony in naturalistic settings: within-family cortisol associations and moderators. J Fam Psychol 23(6):882

    Article  PubMed  PubMed Central  Google Scholar 

  • Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40(3):879–891

    Article  PubMed  Google Scholar 

  • Preacher KJ, Rucker DD, Hayes AF (2007) Addressing moderated mediation hypotheses: theory, methods, and prescriptions. Multivar Behav Res 42(1):185–227

    Article  Google Scholar 

  • Rosmalen JGM, Oldehinkel AJ, Ormel J, De Winter AF, Buitelaar JK, Verhulst FC (2005) Determinants of salivary cortisol levels in 10–12 year old children; a population-based study of individual differences. Psychoneuroendocrinology 30(5):483–495

    Article  CAS  PubMed  Google Scholar 

  • Ruttle PL, Shirtcliff EA, Serbin LA, Fisher DB-D, Stack DM, Schwartzman AE (2011) Disentangling psychobiological mechanisms underlying internalizing and externalizing behaviors in youth: longitudinal and concurrent associations with cortisol. Horm Behav 59(1):123–132

    Article  PubMed  Google Scholar 

  • Saxbe DE, Margolin G, Spies Shapiro L, Ramos M, Rodriguez A, Iturralde E (2014) Relative influences: patterns of HPA axis concordance during triadic family interaction. Health Psychol 33(3):273

    Article  PubMed  Google Scholar 

  • Saxbe D, Del Piero L, Margolin G (2015) Neural correlates of parent–child HPA axis coregulation. Horm behav 75:25–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scher A, Sharabany R (2005) Parenting anxiety and stress: does gender play a part at 3 months of age? J Genet Psychol 166(2):203–214

    Article  PubMed  Google Scholar 

  • Scher CD, Stein MB, Asmundson GJ, McCreary DR, Forde DR (2001) The childhood trauma questionnaire in a community sample: psychometric properties and normative data. J Trauma Stress 14(4):843–857

    Article  CAS  PubMed  Google Scholar 

  • Schreiber JE, Shirtcliff E, Van Hulle C, Lemery-Chalfant K, Klein MH, Kalin NH, Goldsmith HH (2006) Environmental influences on family similarity in afternoon cortisol levels: twin and parent–offspring designs. Psychoneuroendocrinology 31(9):1131–1137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethre-Hofstad L, Stansbury K, Rice MA (2002) Attunement of maternal and child adrenocortical response to child challenge. Psychoneuroendocrinology 27(6):731–747

    Article  CAS  PubMed  Google Scholar 

  • Smith AL, Cross D, Winkler J, Jovanovic T, Bradley B (2014) Emotional dysregulation and negative affect mediate the relationship between maternal history of child maltreatment and maternal child abuse potential. J Fam Violence 29(5):483–494

    Article  Google Scholar 

  • Spinhoven P, Penninx BW, Hickendorff M, van Hemert AM, Bernstein DP, Elzinga BM (2014) Childhood trauma questionnaire: factor structure, measurement invariance, and validity across emotional disorders. Psychol Assess 26(3):717

    Article  PubMed  Google Scholar 

  • Sroufe LA (2000) Early relationships and the development of children. Infant Ment Health J 21(1–2):67–74

    Article  Google Scholar 

  • Suveg C, Shaffer A, Davis M (2016) Family stress moderates relations between physiological and behavioral synchrony and child self-regulation in mother–preschooler dyads. Dev Psychobiol 58(1):83–97

    Article  PubMed  Google Scholar 

  • Tarullo AR, Gunnar MR (2006) Child maltreatment and the developing HPA axis. Horm Behav 50(4):632–639

    Article  PubMed  Google Scholar 

  • Tonmyr L, Draca J, Crain J, MacMillan HL (2011) Measurement of emotional/psychological child maltreatment: a review. Child Abuse Negl 35(10):767–782

    Article  PubMed  Google Scholar 

  • Trickett PK, Noll JG, Susman EJ, Shenk CE, Putnam FW (2010) Attenuation of cortisol across development for victims of sexual abuse. Dev Psychopathol 22(01):165–175

    Article  PubMed  PubMed Central  Google Scholar 

  • Tronick EZ (1989) Emotions and emotional communication in infants. Am Psychol 44(2):112

    Article  CAS  PubMed  Google Scholar 

  • Tronick EZ, Cohn JF (1989) Infant–mother face-to-face interaction: age and gender differences in coordination and the occurrence of miscoordination. Child Dev 60(1):85–92

    Article  CAS  PubMed  Google Scholar 

  • Tronick E, Reck C (2009) Infants of depressed mothers. Harv Rev Psychiatry 17(2):147–156

    Article  PubMed  Google Scholar 

  • Urbán R, Kun B, Farkas J, Paksi B, Kökönyei G, Unoka Z, Demetrovics Z (2014) Bifactor structural model of symptom checklists: SCL-90-R and brief symptom inventory (BSI) in a non-clinical community sample. Psychiatry Res 216(1):146–154

    Article  PubMed  Google Scholar 

  • Van Hulle CA, Shirtcliff EA, Lemery-Chalfant K, Goldsmith HH (2012) Genetic and environmental influences on individual differences in cortisol level and circadian rhythm in middle childhood. Horm Behav 62(1):36–42

    Article  PubMed  PubMed Central  Google Scholar 

  • Vecsei P (1979) Glucocorticoids: cortisol, cortisone, corticosterone, compound S, and their metabolites. In: Jaffe BM, Behrmann HR (eds) Methods Horm Radioimmunoassay. Academic, New York, pp 767–796

    Google Scholar 

  • Weinberg MK, Tronick EZ, Cohn JF, Olson KL (1999) Gender differences in emotional expressivity and self-regulation during early infancy. Dev Psychol 35(1):175

    Article  CAS  PubMed  Google Scholar 

  • Williams SR, Cash E, Daup M, Geronimi EM, Sephton SE, Woodruff-Borden J (2013) Exploring patterns in cortisol synchrony among anxious and nonanxious mother and child dyads: a preliminary study. Biol Psychol 93(2):287–295

    Article  PubMed  Google Scholar 

  • Wolff MS, Ijzendoorn MH (1997) Sensitivity and attachment: a meta-analysis on parental antecedents of infant attachment. Child Dev 68(4):571–591

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the German Research Foundation (DFG, Mo 978/3-2).

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Authors and Affiliations

  1. Translational Psychobiology in Child and Adolescent Psychiatry Section, Department of Child and Adolescent Psychiatry, Centre for Psychosocial Medicine, University of Heidelberg, Blumenstr. 8, 69115, Heidelberg, Germany

    Anna Fuchs & M. Kaess

  2. Department of Child and Adolescent Psychiatry, Centre for Psychosocial Medicine, University of Heidelberg, Blumenstr. 8, 69115, Heidelberg, Germany

    Anna Fuchs, E. Möhler, F. Resch & M. Kaess

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  1. Anna Fuchs
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Correspondence to Anna Fuchs.

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Fuchs, A., Möhler, E., Resch, F. et al. Sex-specific differences in adrenocortical attunement in mothers with a history of childhood abuse and their 5-month-old boys and girls. J Neural Transm 123, 1085–1094 (2016). https://doi.org/10.1007/s00702-016-1525-6

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