Abstract
Associations between mothers’ and children’s cortisol secretion parameters are well established. According to the bio-behavioral synchrony model, these associations reflect influences of the mother–child relationship, the child’s social adjustment, and might also reflect shared genetic dispositions. From the bio-behavioral synchrony model, we predicted a stronger mother–child hair cortisol concentration (HCC) link in mothers showing highly adequate (compared to those showing less adequate) parenting behaviors and in children showing low (compared to those showing high) ADHD symptoms. From a genetic perspective, no such moderator effects, or a stronger mother–child HCC link in children with high ADHD symptoms, can be expected. The study sample consisted of 111 4–5-year-old children (64 of whom screened positive for increased ADHD symptoms) and their mothers. ADHD symptoms were assessed by a clinical interview and parent and teacher questionnaires. Maternal sensitive/responsive parenting behavior was assessed by an at-home behavior observation procedure. In mothers and children, HCC in the most proximal 3-cm scalp hair segment was analyzed using luminescence immunoassay. Overall HCCs of mothers and their children correlated significantly. Maternal sensitivity/responsiveness and child ADHD symptoms proved to be significant moderator variables of this association: High maternal sensitivity/responsiveness and low ADHD symptoms of the child were associated with a stronger mother–child link in HCC. The findings are in line with the bio-behavioral synchrony model in the mother–child relationship, and are less compatible with a genetic perspective. The results might hint at environmental events influencing the development of stress axis functioning in subgroups of preschoolers with high ADHD symptoms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Notes
One of the 111 primary caregivers (defined as the parent who shared the most amount of time with the child) was a father. Because an exclusion of this caregiver–child pair did not alter the results of the presented analyses, the case was left in the sample. In the following, however, we refer to this father as a “mother” for the sake of simplicity of wording.
References
Aiken LS, West SG (1991) Multiple regression: testing and interpreting interactions. Sage, Newbury Park
Atkinson L et al (2013) Maternal sensitivity and infant and mother adrenocortical function across challenges. Psychoneuroendocrinology 38:2943–2951. https://doi.org/10.1016/j.psyneuen.2013.08.001
Baldwin DA, Moses LJ (1996) The ontogeny of social information gathering. Child Dev 67:1915–1939. https://doi.org/10.2307/1131601
Breuer D, Döpfner M (2008) Entwicklung eines Fragebogens zur Erfassung von Aufmerksamkeitsdefizit-/Hyperaktivitätsstörungen (ADHS) bei Vorschulkindern im Eltern- und Erzieherurteil Zeitschrift für Entwicklungspsychologie und Pädagogische. Psychologie 40:40–48. https://doi.org/10.1026/0049-8637.40.1.40
Bright MA, Granger DA, Frick JE (2012) Do infants show a cortisol awakening response? Dev Psychobiol 54:736–743. https://doi.org/10.1002/dev.20617
Christiansen H et al (2011) German validation of the Conners Adult ADHD Rating Scales-self-report (CAARS-S) I: factor structure and normative data. Eur Psychiatry 26:100–107. https://doi.org/10.1016/j.eurpsy.2009.12.024
Chronis AM et al (2007) Maternal depression and early positive parenting predict future conduct problems in young children with attention-deficit/hyperactivity disorder. Dev Psychol 43:70–82. https://doi.org/10.1037/0012-1649.43.1.70
Coghill D, Sonuga-Barke EJ (2012) Annual research review: categories versus dimensions in the classification and conceptualisation of child and adolescent mental disorders—implications of recent empirical study. J Child Psychol Psychiatry 53:469–489. https://doi.org/10.1111/j.1469-7610.2011.02511.x
Daley D (2010) Preschool-Parent Account of Child Symptoms (Pre-Pacs)
Denham SA, Workman E, Cole PM, Weissbrod C, Kendziora KT, Zahn-Waxler C (2000) Prediction of externalizing behavior problems from early to middle childhood: the role of parental socialization and emotion expression. Dev Psychopathol 12:23–45
Denson TF, Spanovic M, Miller N (2009) Cognitive appraisals and emotions predict cortisol and immune responses: a meta-analysis of acute laboratory social stressors and emotion. Inductions Psychol Bull 135:823–853. https://doi.org/10.1037/a0016909
Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355–391. https://doi.org/10.1037/0033-2909.130.3.355
Döpfner M, Schmeck K, Berner W, Lehmkuhl G, Poustka F (1994) Reliability and factorial validity of the Child Behavior Checklist—an analysis of a clinical and field sample. Z Kinder Jugenpsychiatr 22:189–205
Döpfner M, Görtz-Dorten A, Lehmkuhl G (2008) DISYPS-II Diagnostik-System für psychische Störungen nach ICD-10 und DSM-IV für Kinder und Jugendliche—II. Huber, Bern
Faraone SV et al (2015) Attention-deficit/hyperactivity disorder. Nat Rev Dis Primers15020. https://doi.org/10.1038/nrdp.2015.20
Federenko IS, Nagamine M, Hellhammer DH, Wadhwa PD, Wust S (2004) The heritability of hypothalamus pituitary adrenal axis responses to psychosocial stress is context dependent. J Clin Endocrinol Metab 89:6244–6250. https://doi.org/10.1210/jc.2004-0981
Feldman R (2012) Bio-behavioral Synchrony: a model for integrating biological and microsocial behavioral processes in the study of parenting. Parent-Sci Pract 12:154–164. https://doi.org/10.1080/15295192.2012.683342
Feldman R (2017) The neurobiology of human attachments. Trends Cogn Sci 21:80–99. https://doi.org/10.1016/j.tics.2016.11.007
Flom M, St John AM, Meyer JS, Tarullo AR (2017) Infant hair cortisol: associations with salivary cortisol and environmental context. Dev Psychobiol 59:26–38. https://doi.org/10.1002/dev.21449
Görtz-Dorten A, Ise E, Hautmann C, Walter D, Döpfner M (2014) Psychometric properties of a German parent rating scale for Oppositional Defiant and Conduct Disorder (FBB-SSV) in clinical and community samples child. Psychiatry Hum Dev 45:388–397. https://doi.org/10.1007/s10578-013-0409-3
Gray NA, Dhana A, Van Der Vyver L, Van Wyk J, Khumalo NP, Stein DJ (2018) Determinants of hair cortisol concentration in children: a systematic review. Psychoneuroendocrinology 87:204–214. https://doi.org/10.1016/j.psyneuen.2017.10.022
Hautzinger M, Bailer M, Hofmeister D, Keller F (2012) ADS. Allgemeine Depressionsskala. Hogrefe, Göttingen
Hibel LC, Trumbell JM, Mercado E (2014) Work/non-workday differences in mother, child, and mother-child morning cortisol in a sample of working mothers and their children. Early Hum Dev 90:1–7. https://doi.org/10.1016/j.earlhumdev.2013.11.007
Isaksson J, Nilsson KW, Nyberg F, Hogmark A, Lindblad F (2012) Cortisol levels in children with attention-deficit/hyperactivity disorder. J Psychiatr Res 46:1398–1405. https://doi.org/10.1016/j.jpsychires.2012.08.021
Kochanska G (1997) Multiple pathways to conscience for children with different temperaments: from toddlerhood to age 5. Dev Psychol 33:228–240. https://doi.org/10.1037//0012-1649.33.2.228
Liu CH, Fink G, Brentani H, Brentani A (2017) An assessment of hair cortisol among postpartum Brazilian mothers and infants from a high-risk community in SAo Paulo: intra-individual stability and association in mother-infant dyads. Dev Psychobiol 59:916–926. https://doi.org/10.1002/dev.21557
Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445. https://doi.org/10.1038/nrn2639
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 Hum Dev 88:227–232. https://doi.org/10.1016/j.earlhumdev.2011.08.010
Moffitt TE et al (2011) A gradient of childhood self-control predicts health, wealth, and public safety. Proc Natl Acad Sci USA 108:2693–2698. https://doi.org/10.1073/pnas.1010076108
Olsen SL, Sameroff AJ, Kerr DC, Lopez NL, Wellman HM (2005) Developmental foundations of externalizing problems in young children: the role of effortful control. Dev Psychopathol 17:25–45
Ouellette SJ, Russell E, Kryski KR, Sheikh HI, Singh SM, Koren G, Hayden EP (2015) Hair cortisol concentrations in higher- and lower-stress mother-daughter dyads: a pilot study of associations and moderators. Dev Psychobiol 57:519–534. https://doi.org/10.1002/dev.21302
Palumbo RV, Marraccini ME, Weyand LL, Wilder-Smith O, McGee HA, Liu S, Goodwin MS (2017) Interpersonal autonomic physiology: a systematic review of the literature. Personal Soc Psychol Rev 21:99–141
Papp LM, Pendry P, Adam EK (2009) Mother-adolescent physiological synchrony in naturalistic settings: within-family cortisol associations and moderators. J Fam Psychol 23:882–894. https://doi.org/10.1037/a0017147
Pauli-Pott U, Beckmann D (2007) On the association of interparental conflict with developing behavioral inhibition and behavior problems in early childhood. J Fam Psychol 21:529–532. https://doi.org/10.1037/0893-3200.21.3.529
Pauli-Pott U, Mertesacker B, Beckmann D (2004) Predicting the development of infant emotionality from maternal characteristics. Dev Psychopathol 16:19–42. https://doi.org/10.1017/S0954579404040398
Pauli-Pott U, Schloß S, Becker K (2017a) Maternal responsiveness as a predictor of self-regulation development and attention-deficit/hyperactivity symptoms across preschool ages. Child Psychiatry Hum Dev. https://doi.org/10.1007/s10578-017-0726-z
Pauli-Pott U, Schloß S, Ruhl I, Skoluda N, Nater UM, Becker K (2017b) Hair cortisol concentration in preschoolers with attention-deficit/hyperactivity symptoms—roles of gender family adversity. Psychoneuroendocrinology 86:25–33
Polowczyk M, Trautmann-Villalba P, Dinter-Jorg M, Gerhold M, Laucht M, Schmidt MH, Esser G (2000) Auffällige Mutter-Kind-Interaktion im Vorschulalter bei Kindern mit hyperkinetischen und Sozialverhaltensauffälligkeiten. Z Klin Psychol Psychother 29:293–304. https://doi.org/10.1026//0084-5345.29.4.293
Rietschel L et al (2017) Hair cortisol in twins: heritability and genetic overlap with psychological variables and stress-system. Genes Sci Rep 7:15351. https://doi.org/10.1038/s41598-017-11852-3
Rösler M, Retz-Junginger P, Retz W, Stieglitz R-D (2008) HASE Homburger ADHS-Skalen für Erwachsene. Hogrefe, Göttingen
Ruttle PL, Serbin LA, Stack DM, Schwartzman AE, Shirtcliff EA (2011) Adrenocortical attunement in mother-child dyads. Importance of situational behavioral characteristics. Biol Psychol 88:104–111. https://doi.org/10.1016/j.biopsycho.2011.06.014
Saxbe DE, Margolin G, Shapiro LS, Ramos M, Rodriguez A, Iturralde E (2014) Relative influences: patterns of HPA axis concordance during triadic family. Interact Health Psychol 33:273–281. https://doi.org/10.1037/a0033509
Scassellati C, Bonvicini C, Faraone SV, Gennarelli M (2012) Biomarkers and attention-deficit/hyperactivity disorder: a systematic review and meta-analyses. J Am Acad Child Adolesc Psychiatry 51:1003–1019 e1020. https://doi.org/10.1016/j.jaac.2012.08.015
Sethre-Hofstad L, Stansbury K, Rice MA (2002) Attunement of maternal and child adrenocortical response to child challenge. Psychoneuroendocrinology 27:731–747. https://doi.org/10.1016/S0306-4530(01)00077-4
Sonuga-Barke EJS, Dalen L, Remington B (2003) Do executive deficits and delay aversion make independent contributions to preschool attention-deficit/hyperactivity disorder symptoms? J Am Acad Child Adolesc Psychiatry 42:1335–1342 doi. https://doi.org/10.1097/01.chi.0000087564.34977.21
Sonuga-Barke EJS, Koerting J, Smith E, McCann DC, Thompson M (2011) Early detection and intervention for attention-deficit/hyperactivity disorder. Expert Rev Neurother 11:557–563. https://doi.org/10.1586/ern.11.39
Stalder T, Steudte S, Alexander N, Miller R, Gao W, Dettenborn L, Kirschbaum C (2012) Cortisol in hair, body mass index and stress-related measures. Biol Psychol 90:218–223. https://doi.org/10.1016/j.biopsycho.2012.03.010
Stalder T et al (2017) Stress-related and basic determinants of hair cortisol in humans: a meta-analysis. Psychoneuroendocrinology 77:261–274. https://doi.org/10.1016/j.psyneuen.2016.12.017
Taylor E, Schachar R, Thorley G, Wieselberg M (1986) Conduct disorder and hyperactivity: I. Separation of hyperactivity and antisocial conduct in British child psychiatric patients. Br J Psychiatry 149:760–767
Tronick E, Beeghly M (2011) Infants’ meaning-making and the development of mental health. Problems Am Psychol 66:107–119. https://doi.org/10.1037/a0021631
Wenning R (2000) Potential problems with the interpretation of hair analysis results. Forensic Sci Int 107:5–12
Wust S, Federenko IS, Van Rossum EFC, Koper JW, Kumsta R, Entringer S, Hellhammer DH (2004) A psychobiological perspective on genetic determinants of hypothalamus-pituitary-adrenal axis activity. Ann Ny Acad Sci 1032:52–62. https://doi.org/10.1196/annals.1314.005
Funding
This work was supported by a grant from the German Research Foundation (DFG, Be2573/3 − 1,2) to Prof. Dr. Katja Becker and Prof. Dr. Ursula Pauli-Pott.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Schloß, S., Müller, V., Becker, K. et al. Hair cortisol concentration in mothers and their children: roles of maternal sensitivity and child symptoms of attention-deficit/hyperactivity disorder. J Neural Transm 126, 1135–1144 (2019). https://doi.org/10.1007/s00702-018-1944-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-018-1944-7