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Prenatal maternal stress, child internalizing and externalizing symptoms, and the moderating role of parenting: findings from the Norwegian mother, father, and child cohort study

Published online by Cambridge University Press:  25 November 2021

Zahra M. Clayborne Open the ORCID record for Zahra M. Clayborne [Opens in a new window] ,
Wendy Nilsen ,
Fartein Ask Torvik ,
Kristin Gustavson ,
Mona Bekkhus ,
Stephen E. Gilman ,
Golam M. Khandaker ,
Deshayne B. Fell  and
Ian Colman
Zahra M. Clayborne*
Affiliation:
School of Epidemiology and Public Health, University of Ottawa, Ottawa, ON, Canada Centre for Fertility and Health, Norwegian Institute of Public Health, Oslo, Norway
Wendy Nilsen
Affiliation:
Work Research Institute, OsloMet - Oslo Metropolitan University, Oslo, Norway
Fartein Ask Torvik
Affiliation:
Centre for Fertility and Health, Norwegian Institute of Public Health, Oslo, Norway Department of Psychology, University of Oslo, Oslo, Norway
Kristin Gustavson
Affiliation:
Department of Psychology, PROMENTA Research Center, University of Oslo, Oslo, Norway Department of Mental Disorders, Norwegian Institute of Public Health, Oslo, Norway
Mona Bekkhus
Affiliation:
Department of Psychology, PROMENTA Research Center, University of Oslo, Oslo, Norway
Stephen E. Gilman
Affiliation:
Social and Behavioral Sciences Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Rockville, MD, USA Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
Golam M. Khandaker
Affiliation:
Department of Psychiatry, University of Cambridge School of Clinical Medicine, Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Fulbourn, UK MRC Integrative Epidemiology Unit, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK Centre for Academic Mental Health, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK
Deshayne B. Fell
Affiliation:
School of Epidemiology and Public Health, University of Ottawa, Ottawa, ON, Canada Children's Hospital of Eastern Ontario (CHEO) Research Institute, Ottawa, ON, Canada
Ian Colman
Affiliation:
School of Epidemiology and Public Health, University of Ottawa, Ottawa, ON, Canada Centre for Fertility and Health, Norwegian Institute of Public Health, Oslo, Norway
*
Author for correspondence: Zahra M. Clayborne, E-mail: zclay068@uottawa.ca
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Abstract

Background

Few studies have examined how parenting influences the associations between prenatal maternal stress and children's mental health. The objectives of this study were to examine the sex-specific associations between prenatal maternal stress and child internalizing and externalizing symptoms, and to assess the moderating effects of parenting behaviors on these associations.

Methods

This study is based on 15 963 mother–child dyads from the Norwegian Mother, Father, and Child Cohort Study (MoBa). A broad measure of prenatal maternal stress was constructed using 41 self-reported items measured during pregnancy. Three parenting behaviors (positive parenting, inconsistent discipline, and positive involvement) were assessed by maternal report at child age 5 years. Child symptoms of internalizing and externalizing disorders (depression, anxiety, attention-deficit hyperactivity disorder, conduct disorder, and oppositional-defiant disorder) were assessed by maternal report at age 8. Analyses were conducted using structural equation modeling techniques.

Results

Prenatal maternal stress was associated with child internalizing and externalizing symptoms at age 8; associations with externalizing symptoms differed by sex. Associations between prenatal maternal stress and child depression, and conduct disorder and oppositional-defiant disorder in males, became stronger as levels of inconsistent discipline increased. Associations between prenatal maternal stress and symptoms of attention-deficit hyperactivity disorder in females were attenuated as levels of parental involvement increased.

Conclusions

This study confirms associations between prenatal maternal stress and children's mental health outcomes, and demonstrates that these associations may be modified by parenting behaviors. Parenting may represent an important intervention target for improving mental health outcomes in children exposed to prenatal stress.

Keywords

Externalizingfetal programinginternalizingMoBaparentingprenatal stress
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 6 , April 2023 , pp. 2437 - 2447
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Appleyard, K., Egeland, B., van Dulmen, M. H. M., & Sroufe, L. A. (2005). When more is not better: The role of cumulative risk in child behavior outcomes. Journal of Child Psychology and Psychiatry and Allied Disciplines, 46(3), 235–245. doi: 10.1111/j.1469-7610.2004.00351.xCrossRefGoogle Scholar
Bale, T. L. (2011). Sex differences in prenatal epigenetic programing of stress pathways. Stress (Amsterdam, Netherlands), 14(4), 348–356. doi: 10.3109/10253890.2011.586447CrossRefGoogle ScholarPubMed
Bale, T. L., & Epperson, C. N. (2015). Sex differences and stress across the lifespan. Nature Neuroscience, 18(10), 1413–1420. doi: 10.1038/nn.4112CrossRefGoogle ScholarPubMed
Barker, D. J. P. (1990). The fetal and infant origins of adult disease. British Medical Journal, 301(6761), 1111. doi: 10.1136/bmj.301.6761.1111CrossRefGoogle ScholarPubMed
Belsky, J., & van IJzendoorn, M. H. (2017). Genetic differential susceptibility to the effects of parenting. Current Opinion in Psychology, 15, 125–130. doi: 10.1016/J.COPSYC.2017.02.021CrossRefGoogle Scholar
Bergman, K., Sarkar, P., Glover, V., & O'Connor, T. G. (2010). Maternal prenatal cortisol and infant cognitive development: Moderation by infant-mother attachment. Biological Psychiatry, 67(11), 1026–1032. doi: 10.1016/j.biopsych.2010.01.002CrossRefGoogle ScholarPubMed
Birmaher, B., Brent, D. A., Chiappetta, L., Bridge, J., Monga, S., & Baugher, M. (1999). Psychometric properties of the screen for child anxiety related emotional disorders (SCARED): A replication study. Journal of the American Academy of Child and Adolescent Psychiatry, 38(10), 1230–1236. doi: 10.1097/00004583-199910000-00011CrossRefGoogle ScholarPubMed
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. K. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry, 36(4), 545–553. doi: 10.1097/00004583-199704000-00018CrossRefGoogle ScholarPubMed
Cecil, C. A. M., Lysenko, L. J., Jaffee, S. R., Pingault, J. B., Smith, R. G., Relton, C. L., … Barker, E. D. (2014). Environmental risk, oxytocin receptor gene (OXTR) methylation and youth callous-unemotional traits: A 13-year longitudinal study. Molecular Psychiatry, 19(10), 1071–1077. doi: 10.1038/mp.2014.95CrossRefGoogle ScholarPubMed
Clayborne, Z. M., Kingsbury, M., Sampasa-Kinyaga, H., Sikora, L., Lalande, K. M., & Colman, I. (2020). Parenting practices in childhood and depression, anxiety, and internalizing symptoms in adolescence: A systematic review. Social Psychiatry and Psychiatric Epidemiology, 56(4), 619–638. doi: 10.1007/s00127-020-01956-zCrossRefGoogle ScholarPubMed
Cong, X., Hosler, A. S., Tracy, M., & Appleton, A. A. (2020). The relationship between parental involvement in childhood and depression in early adulthood. Journal of Affective Disorders, 273, 173–182.CrossRefGoogle ScholarPubMed
Cortes Hidalgo, A. P., Neumann, A., Bakermans-Kranenburg, M. J., Jaddoe, V. W. V., Rijlaarsdam, J., Verhulst, F. C., … Tiemeier, H. (2018). Prenatal maternal stress and child IQ. Child Development, 91(2), 347–365. doi: 10.1111/cdev.13177CrossRefGoogle ScholarPubMed
Costello, E. J., Worthman, C., Erkanli, A., & Angold, A. (2007). Prediction from low birth weight to female adolescent depression: A test of competing hypotheses. Archives of General Psychiatry, 64(3), 338–344. doi: 10.1001/archpsyc.64.3.338CrossRefGoogle ScholarPubMed
Elgar, F. J., Waschbusch, D. A., Dadds, M. R., & Sigvaldason, N. (2007). Development and validation of a short form of the Alabama Parenting Questionnaire. Journal of Child and Family Studies, 16(2), 243–259. doi: 10.1007/s10826-006-9082-5CrossRefGoogle Scholar
Enders, C. K., & Bandalos, D. L. (2001). The relative performance of full information maximum likelihood estimation for missing data in structural equation models. Structural Equation Modeling, 8(3), 430–457. doi: 10.1207/S15328007SEM0803_5CrossRefGoogle Scholar
Feehan, M., McGee, R., Stanton, W. R., & Silva, P. A. (1991). Strict and inconsistent discipline in childhood: Consequences for adolescent mental health. British Journal of Clinical Psychology, 30(4), 325–331. doi: 10.1111/j.2044-8260.1991.tb00953.xCrossRefGoogle ScholarPubMed
Glover, V., & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology and Behavior, 106(5), 736–740. doi: 10.1016/j.physbeh.2012.02.011CrossRefGoogle ScholarPubMed
Glover, V., O'Connor, T. G., & O'Donnell, K. (2010). Prenatal stress and the programming of the HPA axis. Neuroscience & Biobehavioral Reviews, 35(1), 17–22. doi: 10.1016/J.NEUBIOREV.2009.11.008CrossRefGoogle ScholarPubMed
Grant, K. A., McMahon, C., Reilly, N., & Austin, M. P. (2010). Maternal sensitivity moderates the impact of prenatal anxiety disorder on infant mental development. Early Human Development, 86(9), 551–556. https://doi.org/10.1016/j.earlhumdev.2010.07.004.CrossRefGoogle ScholarPubMed
Hartman, S., & Belsky, J. (2018). Prenatal programming of postnatal plasticity revisited – and extended. Development and Psychopathology, 30(3), 825–842. doi: 10.1017/S0954579418000548CrossRefGoogle ScholarPubMed
Hartman, S., Freeman, S. M., Bales, K. L., & Belsky, J. (2018). Prenatal stress as a risk – and an opportunity – factor. Psychological Science, 29(4), 572–580. doi: 10.1177/0956797617739983CrossRefGoogle Scholar
Hawes, D. J., & Dadds, M. R. (2006). Assessing parenting practices through parent-report and direct observation during parent-training. Journal of Child and Family Studies, 15(5), 554–567. doi: 10.1007/s10826-006-9029-xCrossRefGoogle Scholar
Hu, L., & Bentler, P. M. (1999). Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Structural Equation Modeling, 6(1), 1–55. doi: 10.1080/10705519909540118CrossRefGoogle Scholar
Huizink, A. C., Menting, B., De Moor, M. H. M., Verhage, M. L., Kunseler, F. C., Schuengel, C., & Oosterman, M. (2017). From prenatal anxiety to parenting stress: A longitudinal study. Archives of Women's Mental Health, 20(5), 663–672. doi: 10.1007/s00737-017-0746-5CrossRefGoogle ScholarPubMed
Johnson, P. O., & Neyman, J. (1936). Tests of certain linear hypotheses and their application to some educational problems. Statistical Research Memoirs, 1, 57–93.Google Scholar
Kingsbury, M., Sucha, E., Manion, I., Gilman, S. E., & Colman, I. (2020). Adolescent mental health following exposure to positive and harsh parenting in childhood. Canadian Journal of Psychiatry, 65(6), 392–400. doi: 10.1177/0706743719889551CrossRefGoogle ScholarPubMed
Kingsbury, M., Weeks, M., MacKinnon, N., Evans, J., Mahedy, L., Dykxhoorn, J., & Colman, I. (2016). Stressful life events during pregnancy and offspring depression: Evidence from a prospective cohort study. Journal of the American Academy of Child and Adolescent Psychiatry, 55(8), 709–716. doi: 10.1016/j.jaac.2016.05.014CrossRefGoogle ScholarPubMed
Klein, A., & Moosbrugger, H. (2000). Maximum likelihood estimation of latent interaction effects with the LMS method. Psychometrika, 65(4), 457–474. doi: 10.1007/BF02296338CrossRefGoogle Scholar
Kok, R., Linting, M., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Jaddoe, V. W. V., Hofman, A., … Tiemeier, H. (2013). Maternal sensitivity and internalizing problems: Evidence from two longitudinal studies in early childhood. Child Psychiatry & Human Development, 44(6), 751–765. doi: 10.1007/s10578-013-0369-7CrossRefGoogle ScholarPubMed
Lundervold, A. J., Breivik, K., Posserud, M. B., Stormark, K. M., & Hysing, M. (2013). Symptoms of depression as reported by Norwegian adolescents on the short mood and feelings questionnaire. Frontiers in Psychology, 4, 313. doi: 10.3389/fpsyg.2013.00613CrossRefGoogle ScholarPubMed
MacKinnon, N., Kingsbury, M., Mahedy, L., Evans, J., & Colman, I. (2018). The association between prenatal stress and externalizing symptoms in childhood: Evidence from the Avon longitudinal study of parents and children. Biological Psychiatry, 83(2), 100–108. doi: 10.1016/j.biopsych.2017.07.010CrossRefGoogle ScholarPubMed
Magnus, P., Birke, C., Vejrup, K., Haugan, A., Alsaker, E., Daltveit, A. K., … Stoltenberg, C. (2016). Cohort profile update: The Norwegian mother and child cohort study (MoBa). International Journal of Epidemiology, 45(2), 382–388. doi: 10.1093/ije/dyw029CrossRefGoogle ScholarPubMed
Markham, J. A., Mullins, S. E., & Koenig, J. I. (2013). Periadolescent maturation of the prefrontal cortex is sex-specific and is disrupted by prenatal stress. Journal of Comparative Neurology, 521(8), 1828–1843. doi: 10.1002/cne.23262CrossRefGoogle ScholarPubMed
McDonald, R. P., & Ho, M. H. R. (2002). Principles and practice in reporting structural equation analyses. Psychological Methods, 7(1), 64–82. https://doi.org/10.1037/1082-989X.7.1.64.CrossRefGoogle ScholarPubMed
McLean, M. A., Cobham, V. E., Simcock, G., Lequertier, B., Kildea, S., & King, S. (2020). Childhood anxiety: Prenatal maternal stress and parenting in the QF2011 cohort. Child Psychiatry and Human Development, 52(3), 389–398. doi: 10.1007/s10578-020-01024-2.CrossRefGoogle Scholar
Mezulis, A. H., Hyde, J. S., & Clark, R. (2004). Father involvement moderates the effect of maternal depression during a child's infancy on child behavior problems in kindergarten. Journal of Family Psychology, 18(4), 575–588. doi: 10.1037/0893-3200.18.4.575CrossRefGoogle ScholarPubMed
Nast, I., Bolten, M., Meinlschmidt, G., & Hellhammer, D. H. (2013). How to measure prenatal stress? A systematic review of psychometric instruments to assess psychosocial stress during pregnancy. Paediatric and Perinatal Epidemiology, 27(4), 313–322. doi: 10.1111/ppe.12051CrossRefGoogle Scholar
Nilsen, R. M., Vollset, S. E., Gjessing, H. K., Skjærven, R., Melve, K. K., Schreuder, P., … Magnus, P. (2009). Self-selection and bias in a large prospective pregnancy cohort in Norway. Paediatric and Perinatal Epidemiology, 3(6), 597–608. doi: 10.1111/j.1365-3016.2009.01062.xCrossRefGoogle Scholar
O'Donnell, K., O'Connor, T. G., & Glover, V. (2009). Prenatal stress and neurodevelopment of the child: Focus on the HPA axis and role of the placenta prenatal stress or anxiety predicts neurodevelopmental outcomes in the child. Developmental Neuroscience, 31(4), 285–292. doi: 10.1159/000216539CrossRefGoogle ScholarPubMed
Pitzer, M., Jennen-Steinmetz, C., Esser, G., Schmidt, M. H., & Laucht, M. (2011). Differential susceptibility to environmental influences: The role of early temperament and parenting in the development of externalizing problems. Comprehensive Psychiatry, 52(6), 650–658. doi: 10.1016/j.comppsych.2010.10.017CrossRefGoogle ScholarPubMed
Plant, D. T., Barker, E. D., Waters, C. S., Pawlby, S., & Pariante, C. M. (2013). Intergenerational transmission of maltreatment and psychopathology: The role of antenatal depression. Psychological Medicine, 43(3), 519–528. doi: 10.1017/S0033291712001298CrossRefGoogle ScholarPubMed
Plant, D. T., Pariante, C. M., Sharp, D., & Pawlby, S. (2015). Maternal depression during pregnancy and offspring depression in adulthood: Role of child maltreatment. The British Journal of Psychiatry, 207(3), 213–220. doi: 10.1192/bjp.bp.114.156620CrossRefGoogle ScholarPubMed
Pluess, M., & Belsky, J. (2011). Prenatal programming of postnatal plasticity. Development and Psychopathology, 23(1), 29–38.CrossRefGoogle ScholarPubMed
Reitz, E., Deković, M., & Meijer, A. M. (2006). Relations between parenting and externalizing and internalizing problem behaviour in early adolescence: Child behaviour as moderator and predictor. Journal of Adolescence, 29(3), 419–436. doi: 10.1016/j.adolescence.2005.08.003CrossRefGoogle ScholarPubMed
Rijlaarsdam, J., Pappa, I., Walton, E., Bakermans-Kranenburg, M. J., Mileva-Seitz, V. R., Rippe, R. C. A., … van IJzendoorn, M. H. (2016). An epigenome-wide association meta-analysis of prenatal maternal stress in neonates: A model approach for replication. Epigenetics, 11(2), 140–149. doi: 10.1080/15592294.2016.1145329CrossRefGoogle Scholar
Schechter, J. C., Brennan, P. A., Smith, A. K., Stowe, Z. N., Newport, D. J., & Johnson, K. C. (2017). Maternal prenatal psychological distress and preschool cognitive functioning: The protective role of positive parental engagement. Journal of Abnormal Child Psychology, 45(2), 249–260. doi: 10.1007/s10802-016-0161-9CrossRefGoogle ScholarPubMed
Schreuder, P., & Alsaker, E. (2014). The Norwegian mother and child cohort study (MoBa) – MoBa recruitment and logistics. Norsk Epidemiologi, 24(1–2), 23–27. doi: 10.5324/nje.v24i1-2.1754CrossRefGoogle Scholar
Sharp, H., Hill, J., Hellier, J., & Pickles, A. (2015). Maternal antenatal anxiety, postnatal stroking and emotional problems in children: Outcomes predicted from pre- and postnatal programming hypotheses. Psychological Medicine, 45(2), 269–283. doi: 10.1017/S0033291714001342CrossRefGoogle ScholarPubMed
Silva, R. R., Alpert, M., Pouget, E., Silva, V., Trosper, S., Reyes, K., & Dummit, S. (2005). A rating scale for disruptive behavior disorders, based on the DSM-IV item pool. Psychiatric Quarterly, 76(4), 327–339. doi: 10.1007/s11126-005-4966-xCrossRefGoogle ScholarPubMed
Slopen, N., McLaughlin, K. A., & Shonkoff, J. P. (2014). Interventions to improve cortisol regulation in children: A systematic review. Pediatrics, 133(2), 312–326. doi: 10.1542/peds.2013-1632CrossRefGoogle ScholarPubMed
Strand, B. H., Dalgard, O. S., Tambs, K., & Rognerud, M. (2003). Measuring the mental health status of the Norwegian population: A comparison of the instruments SCL-25, SCL-10, SCL-5 and MHI-5 (SF-36). Nordic Journal of Psychiatry, 57(2), 113–118. doi: 10.1080/08039480310000932CrossRefGoogle ScholarPubMed
Sutherland, S., & Brunwasser, S. M. (2018). Sex differences in vulnerability to prenatal stress: A review of the recent literature. Current Psychiatry Reports, 20(11), 1–12. doi: 10.1007/s11920-018-0961-4CrossRefGoogle Scholar
Traub, F., & Boynton-Jarrett, R. (2017). Modifiable resilience factors to childhood adversity for clinical pediatric practice. Pediatrics, 139(5), e20162569. doi: 10.1542/PEDS.2016-2569CrossRefGoogle ScholarPubMed
Van Den Bergh, B. R. H., & Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Development, 75(4), 1085–1097. doi: 10.1111/j.1467-8624.2004.00727.xCrossRefGoogle ScholarPubMed
Van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., Braeken, M., de Rooij, S. R., Entringer, S., … Schwab, M. (2017). Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience and Biobehavioral Reviews, 117, 26–64. doi: 10.1016/j.neubiorev.2017.07.003CrossRefGoogle ScholarPubMed
Williford, A. P., Calkins, S. D., & Keane, S. P. (2007). Predicting change in parenting stress across early childhood: Child and maternal factors. Journal of Abnormal Child Psychology, 35(2), 251–263. doi: 10.1007/s10802-006-9082-3CrossRefGoogle ScholarPubMed
Yap, M. B. H., Cheong, T. W. K., Zaravinos-Tsakos, F., Lubman, D. I., & Jorm, A. F. (2017). Modifiable parenting factors associated with adolescent alcohol misuse: A systematic review and meta-analysis of longitudinal studies. Addiction, 112(7), 1142–1162. doi: 10.1111/add.13785CrossRefGoogle ScholarPubMed
Yap, M. B. H., Morgan, A. J., Cairns, K., Jorm, A. F., Hetrick, S. E., & Merry, S. (2016). Parents in prevention: A meta-analysis of randomized controlled trials of parenting interventions to prevent internalizing problems in children from birth to age 18. Clinical Psychology Review, 50, 138–158. doi: 10.1016/j.cpr.2016.10.003CrossRefGoogle ScholarPubMed
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