Abstract
Children now are facing an increasing risk of early life stress (ELS), which leads to detrimental psychosocial outcomes. Behavior studies suggested that positive parental interactions might moderate the negative impact of ELS, but the related biological alteration remains unclear. This study aims to investigate whether positive parent–child interactions moderate the association between maltreatment (as a severe form of ELS) and hair cortisol concentration (HCC), as well as between HCC and psychosocial outcomes in young children. Participants were 6-year-old Chinese children (N = 257, Mage = 6.2, 121 were male) selected by stratified cluster random sampling from a Shanghai population representative cohort. Proximal 3 cm hair strands were analyzed using liquid chromatography coupled with tandem mass spectrometry for HCC. Children’s psychosocial outcome was evaluated using the parental report Strengths and Difficulties Questionnaire (SDQ). Parents also reported the frequency of positive parent–child interactions using the Chinese Parent–Child Interaction Scale (CPCIS) as well as the history of maltreatment. Multi-level logistic regression models adjusting for individual, kindergarten, and district confounders were used to evaluate the associations between maltreatment, HCC, and psychosocial outcomes. Interactions terms tested whether more frequent positive parent–child interactions moderates the association between maltreatment and HCC, as well as between HCC and psychosocial outcomes. Maltreated children exhibited higher levels of HCC (B = 1.20, 95% CI: 0.38,2.02; p = 0.004), and children with higher HCC exhibited poorer psychosocial outcomes (B = 0.34, 95% CI: 0.18,0.51; p < 0.001). Positive parent–child interactions did not have a moderating effect on the association between maltreatment and HCC, but they demonstrated a moderating effect on the association between increased HCC and psychosocial outcomes (interaction term: B = −0.42, 95% CI: −0.75,−0.10; p = 0.01). These findings provide evidence that positive parental interaction may serve as a moderator between chronic cortisol exposure and psychosocial problems. It highlights the importance of frequent parent–child interactions, especially among children under a high risk of ELS.
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Availability of data and materials
The datasets generated and/or analyzed during the current study are not publicly available due to shared ownership of Shanghai Municipal Education Commission but are available from the corresponding author on reasonable request.
Abbreviations
- HCC:
-
Hair cortisol concentration
- ELS:
-
Early life stress
- SDQ:
-
Strengths and Difficulties Questionnaire
- CPCIS:
-
Chinese Parent–Child Interaction Scale
References
Nelson CA, Scott RD, Bhutta ZA, Harris NB, Danese A, Samara M (2020) Adversity in childhood is linked to mental and physical health throughout life. BMJ 371:m3048
Boeldt DL, Rhee SH, Dilalla LF, Mullineaux PY, Schulz-Heik RJ, Corley RP, Young SE, Hewitt JK (2012) The association between positive parenting and externalizing behavior. Infant Child Dev 21(1):85–106
Garner AS, Shonkoff JP, Committee on Psychosocial Aspects of Child and Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics (2012) Early childhood adversity, toxic stress, and the role of the pediatrician: translating developmental science into lifelong health. Pediatrics 129(1):e224–e231
Tooley UA, Bassett DS, Mackey AP (2021) Environmental influences on the pace of brain development. Nat Rev Neurosci 22(6):372–384
Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P, Richter L, Strupp B (2007) Developmental potential in the first 5 years for children in developing countries. Lancet 369(9555):60–70
Jiang Z, Xu H, Wang S, Gao X, Li S, Zhang S, Tao F, Wan Y (2022) Parent-child relationship quality, childhood maltreatment, and psychological symptoms in Chinese adolescent. J Interpers Violence 37(19–20):NP18130–NP18151
Fagan AA (2020) Child maltreatment and aggressive behaviors in early adolescence: evidence of moderation by parent/child relationship quality. Child Maltreat 25(2):182–191
Corlis M, Damashek A (2021) Examining parental factors as moderators between maltreatment and adolescent delinquency. J Interpers Violence 36(17–18):NP9391–NP9415
Yoon S, Yoon D, Latelle A, Kobulsky JM (2022) The interaction effects between father-child relationship quality and parent-perpetrated maltreatment on adolescent behavior problems. J Interpers Violence 37(17–18):NP15944–NP15969
Russell G, Lightman S (2019) The human stress response. Nat Rev Endocrinol 15(9):525–534
Graß J, Kirschbaum C, Miller R, Gao W, Steudte-Schmiedgen S, Stalder T (2015) Sweat-inducing physiological challenges do not result in acute changes in hair cortisol concentrations. Psychoneuroendocrinology 61:64
Short SJ, Stalder T, Marceau K, Entringer S, Moog NK, Shirtcliff EA, Wadhwa PD, Buss C (2016) Correspondence between hair cortisol concentrations and 30-day integrated daily salivary and weekly urinary cortisol measures. Psychoneuroendocrinology 71:12–18
Stalder T, Steudte S, Miller R, Skoluda N, Dettenborn L, Kirschbaum C (2012) Intraindividual stability of hair cortisol concentrations. Psychoneuroendocrinology 37(5):602–610
Lee DY, Kim E, Choi MH (2015) Technical and clinical aspects of cortisol as a biochemical marker of chronic stress. BMB Rep 48(4):209–216
LeMoult J, Humphreys KL, Tracy A, Hoffmeister JA, Ip E, Gotlib IH (2020) Meta-analysis: exposure to early life stress and risk for depression in childhood and adolescence. J Am Acad Child Adolesc Psychiatry 59(7):842–855
Karlén J, Ludvigsson J, Hedmark M, Faresjö Å, Theodorsson E, Faresjö T (2015) Early psychosocial exposures, hair cortisol levels, and disease risk. Pediatrics 135(6):e1450–e1457
Bhopal S, Verma D, Roy R, Soremekun S, Kumar D, Bristow M, Bhanushali A, Divan G, Kirkwood B (2019) The contribution of childhood adversity to cortisol measures of early life stress amongst infants in rural India: findings from the early life stress sub-study of the SPRING cluster randomised controlled trial (SPRING-ELS). Psychoneuroendocrinology 107:241–250
Groeneveld MG, Vermeer HJ, Linting M, Noppe G, van Rossum EF, van IJzendoorn MH (2013) Children’s hair cortisol as a biomarker of stress at school entry. Stress 16(6):711–715
Luo H, Hu X, Liu X, Ma X, Guo W, Qiu C, Wang Y, Wang Q, Zhang X, Zhang W, Hannum G, Zhang K, Liu X, Li T (2012) Hair cortisol level as a biomarker for altered hypothalamic-pituitary-adrenal activity in female adolescents with posttraumatic stress disorder after the 2008 Wenchuan earthquake. Biol Psychiatry 72(1):65–69
Simmons JG, Badcock PB, Whittle SL, Byrne ML, Mundy L, Patton GC, Olsson CA, Allen NB (2016) The lifetime experience of traumatic events is associated with hair cortisol concentrations in community-based children. Psychoneuroendocrinology 63:276–281
White LO, Ising M, von Klitzing K, Sierau S, Michel A, Klein AM, Andreas A, Keil J, Quintero L, Muller-Myhsok B, Uhr M, Gausche R, Manly JT, Crowley MJ, Kirschbaum C, Stalder T (2017) Reduced hair cortisol after maltreatment mediates externalizing symptoms in middle childhood and adolescence. J Child Psychol Psychiatry 58(9):998–1007
Bryson HE, Mensah F, Goldfeld S, Price AMH (2020) Using hair cortisol to examine the role of stress in children’s health inequalities at 3 years. Acad Pediatr 20(2):193–202
Kornelsen E, Buchan MC, Gonzalez A, Ferro MA (2019) Hair cortisol concentration and mental disorder in children with chronic physical illness. Chronic Stress (Thousand Oaks) 3:2470547019875116
Perry NB, Donzella B, Troy MF, Barnes AJ (2022) Mother and child hair cortisol during the COVID-19 pandemic: associations among physiological stress, pandemic-related behaviors, and child emotional-behavioral health. Psychoneuroendocrinology 137:105656
Moriceau S, Sullivan RM (2006) Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 9(8):1004–1006
Albers EM, Riksen-Walraven JM, Sweep FC, de Weerth C (2008) Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. J Child Psychol Psychiatry 49(1):97–103
Gunnar MR (2017) Social buffering of stress in development: a career perspective. Perspect Psychol Sci 12(3):355–373
Nachmias M, Gunnar M, Mangelsdorf S, Parritz RH, Buss K (1996) Behavioral inhibition and stress reactivity: the moderating role of attachment security. Child Dev 67(2):508–522
Gunnar MR, Brodersen L, Nachmias M, Buss K, Rigatuso J (1996) Stress reactivity and attachment security. Dev Psychobiol 29(3):191–204
Nofech-Mozes J, Pereira J, Gonzalez A, Atkinson L (2019) Cortisol secretion moderates the association between mother-infant attachment at 17 months and child behavior at age 5 years. Dev Psychobiol 61(2):239–253
Wang X, Zhang Y, Zhao J, Shan W, Zhang Z, Wang G, Jiang Y, Zhu W, Zhang D, He Y, Mao H, Qu J, Zhu Q, Jiang F (2021) Cohort profile: the Shanghai Children’s Health, Education and Lifestyle Evaluation, Preschool (SCHEDULE-P) study. Int J Epidemiol 50(2):391–399
Shan W, Zhang Y, Zhao J, Zhang Y, Cheung EFC, Chan RCK, Jiang F (2019) Association between maltreatment, positive parent-child interaction, and psychosocial well-being in young children. J Pediatr 213:180–186.e1
Greff MJE, Levine JM, Abuzgaia AM, Elzagallaai AA, Rieder MJ, van Uum SHM (2019) Hair cortisol analysis: an update on methodological considerations and clinical applications. Clin Biochem 63:1–9
Gao W, Stalder T, Foley P, Rauh M, Deng H, Kirschbaum C (2013) Quantitative analysis of steroid hormones in human hair using a column-switching LC-APCI-MS/MS assay. J Chromatogr B Analyt Technol Biomed Life Sci 928:1–8
Ip P, Tso W, Rao N, Ho FKW, Chan KL, Fu KW, Li SL, Goh W, Wong WH, Chow CB (2018) Rasch validation of the Chinese parent-child interaction scale (CPCIS). World J Pediatr 14(3):238–246
Zhao J, Zhang Y, Jiang F, Ip P, Ho FKW, Zhang Y, Huang H (2018) Excessive screen time and psychosocial well-being: the mediating role of body mass index, sleep duration, and parent-child interaction. J Pediatr 202:157–162.e1
Goodman R (1997) The Strengths and Difficulties Questionnaire: a research note. J Child Psychol Psychiatry 38(5):581–586
Kou JH, Du YS, Xia LM (2005) Reliability and validity of ‘children strengths and difficulties questionnaire’ in Shanghai norm. Shanghai Arch Psychiatry 17:25–28
Salum GA, DeSousa DA, Manfro GG, Pan PM, Gadelha A, Brietzke E, Miguel EC, Mari JJ, do Rosário MC, Grassi-Oliveira R (2016) Measuring child maltreatment using multi-informant survey data: a higher-order confirmatory factor analysis. Trends Psychiatry Psychother 38(1):23–32
Rippe RC, Noppe G, Windhorst DA, Tiemeier H, van Rossum EF, Jaddoe VW, Verhulst FC, Bakermans-Kranenburg MJ, van IJzendoorn MH, van den Akker EL (2016) Splitting hair for cortisol? Associations of socio-economic status, ethnicity, hair color, gender and other child characteristics with hair cortisol and cortisone. Psychoneuroendocrinology 66:56–64
van der Vegt EJM, van der Ende J, Kirschbaum C, Verhulst FC, Tiemeier H (2009) Early neglect and abuse predict diurnal cortisol patterns in adults. Psychoneuroendocrinology 34(5):660–669
Steudte S, Kirschbaum C, Gao W, Alexander N, Schonfeld S, Hoyer J, Stalder T (2013) Hair cortisol as a biomarker of traumatization in healthy individuals and posttraumatic stress disorder patients. Biol Psychiatry 74(9):639–646
Fries E, Hesse J, Hellhammer J, Hellhammer DH (2005) A new view on hypocortisolism. Psychoneuroendocrinology 30(10):1010–1016
Kim J, Li L, Korous KM, Valiente C, Tsethlikai M (2022) Chronic stress predicts post-traumatic stress disorder symptoms via executive function deficits among urban American Indian children. Stress 25(1):97–104
Koumantarou Malisiova E, Mourikis I, Darviri C, Nicolaides NC, Zervas IM, Papageorgiou C, Chrousos GP (2021) Hair cortisol concentrations in mental disorders: a systematic review. Physiol Behav 229:113244
Herane Vives A, De Angel V, Papadopoulos A, Strawbridge R, Wise T, Young AH, Arnone D, Cleare AJ (2015) The relationship between cortisol, stress and psychiatric illness: new insights using hair analysis. J Psychiatr Res 70:38–49
Wei J, Sun G, Zhao L, Yang X, Liu X, Lin D, Li T, Ma X (2015) Analysis of hair cortisol level in first-episodic and recurrent female patients with depression compared to healthy controls. J Affect Disord 175:299–302
Coello K, Munkholm K, Nielsen F, Vinberg M, Kessing LV (2019) Hair cortisol in newly diagnosed bipolar disorder and unaffected first-degree relatives. Psychoneuroendocrinology 99:183–190
Mewes R, Reich H, Skoluda N, Seele F, Nater UM (2017) Elevated hair cortisol concentrations in recently fled asylum seekers in comparison to permanently settled immigrants and non-immigrants. Transl Psychiatry 7(3):e1051
Steudte-Schmiedgen S, Stalder T, Schönfeld S, Wittchen HU, Trautmann S, Alexander N, Miller R, Kirschbaum C (2015) Hair cortisol concentrations and cortisol stress reactivity predict PTSD symptom increase after trauma exposure during military deployment. Psychoneuroendocrinology 59:123–133
Tallo-Parra O, Lopez-Bejar M, Carbajal A, Monclús L, Manteca X, Devant M (2017) Acute ACTH-induced elevations of circulating cortisol do not affect hair cortisol concentrations in calves. Gen Comp Endocrinol 240:138–142
Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9(1):46–56
Raison CL, Capuron L, Miller AH (2006) Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 27(1):24–31
Pervanidou P, Kolaitis G, Charitaki S, Margeli A, Ferentinos S, Bakoula C, Lazaropoulou C, Papassotiriou I, Tsiantis J, Chrousos GP (2007) Elevated morning serum interleukin (IL)-6 or evening salivary cortisol concentrations predict posttraumatic stress disorder in children and adolescents six months after a motor vehicle accident. Psychoneuroendocrinology 32(8–10):991–999
Olff M, Frijling JL, Kubzansky LD, Bradley B, Ellenbogen MA, Cardoso C, Bartz JA, Yee JR, van Zuiden M (2013) The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38(9):1883–1894
Clodi M, Vila G, Geyeregger R, Riedl M, Stulnig TM, Struck J, Luger TA, Luger A (2008) Oxytocin alleviates the neuroendocrine and cytokine response to bacterial endotoxin in healthy men. Am J Physiol Endocrinol Metab 295(3):E686–E691
Feldman R, Golan O, Hirschler-Guttenberg Y, Ostfeld-Etzion S, Zagoory-Sharon O (2014) Parent-child interaction and oxytocin production in pre-schoolers with autism spectrum disorder. Br J Psychiatry 205(2):107–112
Engle PL, Fernald LCH, Alderman H, Behrman J, O’Gara C, Yousafzai A, de Mello MC, Hidrobo M, Ulkuer N, Ertem I, Iltus S (2011) Strategies for reducing inequalities and improving developmental outcomes for young children in low-income and middle-income countries. Lancet 378(9799):1339–1353
Milner JS, Crouch JL (1997) Impact and detection of response distortions on parenting measures used to assess risk for child physical abuse. J Pers Assess 69(3):633–650
Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17(2):271–301
Acknowledgements
Study statistical expert: Dr. Hao Pan.
Funding
Supported by National Natural Science Foundation of China (82103866), Shanghai Municipal Health Commission (20214Y0112), Shanghai Municipal Education Commission (2022you1-2, D1502), The Innovative Research Team of High-level Local Universities in Shanghai (SHSMU-ZDCX20211900).
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WS, YZ and FJ took the initiative in conception and design, and WS analyzed the data and complete the draft of the manuscript. WS, YZ, JZ collected the data and provide critical suggestions on data analysis. FJ, LZ, BJH, and JDT made substantial contributions to the interpretation of data and manuscript revision. All authors reviewed the manuscript.
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The study received approval from the institutional review board of the Shanghai Children’s Medical Center, Shanghai Jiao Tong University (SCMCIRB-K2016022-01). Parents of the involved children signed the informed consent before participating in the study.
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Shan, W., Zhang, Y., Zhao, J. et al. Association between maltreatment, hair cortisol concentration, positive parent–child interaction, and psychosocial outcomes in Chinese preschool children. Eur Child Adolesc Psychiatry (2024). https://doi.org/10.1007/s00787-023-02355-w
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DOI: https://doi.org/10.1007/s00787-023-02355-w