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The persisting effect of maternal mood in pregnancy on childhood psychopathology

Published online by Cambridge University Press:  12 March 2014

Kieran J. O'Donnell ,
Vivette Glover ,
Edward D. Barker  and
Thomas G. O'Connor
Kieran J. O'Donnell
Affiliation:
McGill University
Vivette Glover
Affiliation:
Imperial College London
Edward D. Barker
Affiliation:
Birkbeck University
Thomas G. O'Connor*
Affiliation:
University of Rochester Medical Center
*
Address correspondence and reprint requests to: Thomas G. O'Connor, Department of Psychiatry, Wynne Center for Family Research, University of Rochester Medical Center, 300 Crittenden Boulevard, Rochester, NY 14642; E-mail: [email protected].
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Abstract

Developmental or fetal programming has emerged as a major model for understanding the early and persisting effects of prenatal exposures on the health and development of the child and adult. We leverage the power of a 14-year prospective study to examine the persisting effects of prenatal anxiety, a key candidate in the developmental programming model, on symptoms of behavioral and emotional problems across five occasions of measurement from age 4 to 13 years. The study is based on the Avon Longitudinal Study of Parents and Children cohort, a prospective, longitudinal study of a large community sample in the west of England (n = 7,944). Potential confounders included psychosocial and obstetric risk, postnatal maternal mood, paternal pre- and postnatal mood, and parenting. Results indicated that maternal prenatal anxiety predicted persistently higher behavioral and emotional symptoms across childhood with no diminishment of effect into adolescence. Elevated prenatal anxiety (top 15%) was associated with a twofold increase in risk of a probable child mental disorder, 12.31% compared with 6.83%, after allowing for confounders. Results were similar with prenatal depression. These analyses provide some of the strongest evidence to date that prenatal maternal mood has a direct and persisting effect on her child's psychiatric symptoms and support an in utero programming hypothesis.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Issue 2 , May 2014 , pp. 393 - 403
Copyright
Copyright © Cambridge University Press 2014 

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References

Alderman, K. J., Mackay, C. J., Lucas, E. G., Spry, W. B., & Bell, B. (1983). Factor analysis and reliability studies of the Crown–Crisp Experiential Index (CCEI). British Journal of Medical Psychology, 56 (Pt. 4), 329–345.CrossRefGoogle ScholarPubMed
Allen, G. (2011). Early intervention: The next steps. London: HM Government.Google Scholar
Barker, D. J. (1999). Fetal origins of cardiovascular disease. Annals Medicine, 31(Suppl. 1), 3–6.CrossRefGoogle ScholarPubMed
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, 1026–1032. doi:10.1016/j.biopsych.2010.01.002 CrossRefGoogle ScholarPubMed
Bergman, K., Sarkar, P., O'Connor, T. G., Modi, N., & Glover, V. (2007). Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. Journal of the American Academy of Child & Adolescent Psychiatry, 46, 1454–1463. doi:10.1097/chi.0b013e31814a62f6 Google Scholar
Bick, J., Naumova, O., Hunter, S., Barbot, B., Lee, M., Luthar, S. S., et al. (2012). Childhood adversity and DNA methylation of genes involved in the hypothalamus–pituitary–adrenal axis and immune system: Whole-genome and candidate-gene associations. Development and Psychopathology, 24, 1417–1425. doi:10.1017/S0954579412000806 Google Scholar
Birtchnell, J., Evans, C., & Kennard, J. (1988). The total score of the Crown–Crisp Experiential Index: A useful and valid measure of psychoneurotic pathology. British Journal Medical Psychology, 61(Pt. 3), 255–266.CrossRefGoogle ScholarPubMed
Braithwaite, E. C., Ramchandani, P. G., O'Connor, T. G., van Ijzendoorn, M. H., Bakermans-Kranenburg, M. J., Glover, V., et al. (2013). No moderating effect of 5-HTTLPR on associations between antenatal anxiety and infant behavior. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 519–526. doi:10.1016/j.jaac.2013.02.010 CrossRefGoogle ScholarPubMed
Buitelaar, J. K., Huizink, A. C., Mulder, E. J., de Medina, P. G., & Visser, G. H. (2003). Prenatal stress and cognitive development and temperament in infants. Neurobiology of Aging, 24(Suppl. 1), S53–S60; discussion S67–S58. doi:S0197458003000502 CrossRefGoogle ScholarPubMed
Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010). High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology, 35, 141–153. doi:10.1016/j.psyneuen.2009.07.010 CrossRefGoogle ScholarPubMed
Coe, C. L., Kramer, M., Czeh, B., Gould, E., Reeves, A. J., Kirschbaum, C., et al. (2003). Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biological Psychiatry, 54, 1025–1034. doi:S000632230300698X CrossRefGoogle ScholarPubMed
Costello, E. J., Copeland, W., & Angold, A. (2011). Trends in psychopathology across the adolescent years: What changes when children become adolescents, and when adolescents become adults? Journal of Child Psychology and Psychiatry, and Allied Disciplines, 52, 1015–1025. doi:10.1111/j.1469-7610.2011.02446.x Google Scholar
Costello, E. J., Mustillo, S., Erkanli, A., Keeler, G., & Angold, A. (2003). Prevalence and development of psychiatric disorders in childhood and adolescence. Archive of General Psychiatry, 60, 837–844. doi:10.1001/archpsyc.60.8.837 CrossRefGoogle ScholarPubMed
Cox, J. L., Holden, J. M., & Sagovsky, R. (1987). Detection of postnatal depression: Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry, 150, 782–786.CrossRefGoogle ScholarPubMed
Dahl, R. E., & Gunnar, M. R. (2009). Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 1–6. doi:10.1017/S0954579409000017 Google Scholar
Davis, E. P., Glynn, L. M., Waffarn, F., & Sandman, C. A. (2011). Prenatal maternal stress programs infant stress regulation. Journal of Child Psychology Psychiatry, 52, 119–129. doi:10.1111/j.1469-7610.2010.02314.x CrossRefGoogle ScholarPubMed
Fisher, P. A., Lester, B. M., DeGarmo, D. S., Lagasse, L. L., Lin, H., Shankaran, S., et al. (2011). The combined effects of prenatal drug exposure and early adversity on neurobehavioral disinhibition in childhood and adolescence. Development and Psychopathology, 23, 777–788. doi:10.1017/S0954579411000290 CrossRefGoogle ScholarPubMed
Ford, T., Goodman, R., & Meltzer, H. (2003). The British Child and Adolescent Mental Health Survey 1999: The prevalence of DSM-IV disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 42, 1203–1211.CrossRefGoogle ScholarPubMed
Gale, C. R., O'Callaghan, F. J., Bredow, M., & Martyn, C. N. (2006). The influence of head growth in fetal life, infancy, and childhood on intelligence at the ages of 4 and 8 years. Pediatrics, 118, 1486–1492. doi:10.1542/peds.2005-2629 CrossRefGoogle ScholarPubMed
Gillman, M. W., Barker, D., Bier, D., Cagampang, F., Challis, J., Fall, C., et al. (2007). Meeting report on the 3rd International Congress on Developmental Origins of Health and Disease (DOHaD). Pediatric Research, 61(5 Pt 1), 625–629. doi:10.1203/pdr.0b013e3180459fcd CrossRefGoogle ScholarPubMed
Glover, V., O'Connor, T. G., Heron, J., & Golding, J. (2004). Antenatal maternal anxiety is linked with atypical handedness in the child. Early Human Development, 79, 107–118. doi:10.1016/j.earlhumdev.2004.04.012 S0378-3782(04)00072-6 CrossRefGoogle ScholarPubMed
Gluckman, P. D., & Hanson, M. A. (2004). Developmental origins of disease paradigm: A mechanistic and evolutionary perspective. Pediatric Research, 56, 311–317. doi:10.1203/01.PDR.0000135998.08025.FB01.PDR.0000135998.08025.FB CrossRefGoogle ScholarPubMed
Golding, J., Pembrey, M., & Jones, R. (2001). ALSPAC—The Avon Longitudinal Study of Parents and Children: I. Study methodology. Paediatric and Perinatal Epidemiology, 15, 74–87.Google Scholar
Goodman, A., & Goodman, R. (2011). Population mean scores predict child mental disorder rates: Validating SDQ prevalence estimators in Britain. Journal of Child Psychology and Psychiatry, 52, 100–108. doi:10.1111/j.1469-7610.2010.02278.x Google Scholar
Goodman, R., Meltzer, H., & Bailey, V. (1998). The Strengths and Difficulties Questionnaire: A pilot study on the validity of the self-report version. European Child & Adolescent Psychiatry, 7, 125–130. doi:10.1007/s007870050057 CrossRefGoogle ScholarPubMed
Hansen, D., Lou, H. C., & Olsen, J. (2000). Serious life events and congenital malformations: A national study with complete follow-up. Lancet, 356, 875–880. doi:10.1016/S0140-6736(00)02676-3 Google Scholar
Heron, J., O'Connor, T. G., Evans, J., Golding, J., & Glover, V. (2004). The course of anxiety and depression through pregnancy and the postpartum in a community sample. Journal of Affective Disorders, 80, 65–73. doi:10.1016/j.jad.2003.08.004S0165032703002064 Google Scholar
Hu, L.-T., & Bentler, P. M. (1999). Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal, 6, 1–55.Google Scholar
Huizink, A. C., Mulder, E. J., & Buitelaar, J. K. (2004). Prenatal stress and risk for psychopathology: Specific effects or induction of general susceptibility? Psychological Bulletin, 130, 115–142. doi:10.1037/0033-2909.130.1.1152003-11000-005 CrossRefGoogle ScholarPubMed
Khashan, A. S., Abel, K. M., McNamee, R., Pedersen, M. G., Webb, R. T., Baker, P. N., et al. (2008). Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Archies of General Psychiatry, 65, 146–152. doi:10.1001/archgenpsychiatry.2007.20 CrossRefGoogle ScholarPubMed
Kim-Cohen, J., Caspi, A., Moffitt, T. E., Harrington, H., Milne, B. J., & Poulton, R. (2003). Prior juvenile diagnoses in adults with mental disorder: Developmental follow-back of a prospective-longitudinal cohort. Archives of General Psychiatry, 60, 709–717. doi:10.1001/archpsyc.60.7.70960/7/709 Google Scholar
King, S., Mancini-Marie, A., Brunet, A., Walker, E., Meaney, M. J., & Laplante, D. P. (2009). Prenatal maternal stress from a natural disaster predicts dermatoglyphic asymmetry in humans. Development and Psychopathology, 21, 343–353. doi:10.1017/S0954579409000364 CrossRefGoogle ScholarPubMed
Kinney, D. K., Miller, A. M., Crowley, D. J., Huang, E., & Gerber, E. (2008). Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. Journal of Autism Developmental Disorders, 38, 481–488.CrossRefGoogle ScholarPubMed
Liu, J., Portnoy, J., & Raine, A. (2012). Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children. Development and Psychopathology, 24, 771–782. doi:10.1017/S0954579412000363 Google Scholar
Maccari, S., Darnaudery, M., Morley-Fletcher, S., Zuena, A. R., Cinque, C., & Van Reeth, O. (2003). Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neuroscience and Biobehavior Review, 27, 119–127. doi:S0149763403000149 Google Scholar
Melhuish, E., Belsky, J., Leyland, A. H., & Barnes, J. (2008). Effects of fully-established Sure Start Local Programmes on 3-year-old children and their families living in England: A quasi-experimental observational study. Lancet, 372, 1641–1647. doi:10.1016/S0140-6736(08)61687-6 CrossRefGoogle Scholar
Monk, C., Spicer, J., & Champagne, F. A. (2012). Linking prenatal maternal adversity to developmental outcomes in infants: The role of epigenetic pathways. Development and Psychopathology, 24, 1361–1376. doi:10.1017/S0954579412000764 Google Scholar
Murray, L., Arteche, A., Fearon, P., Halligan, S., Goodyer, I., & Cooper, P. (2011). Maternal postnatal depression and the development of depression in offspring up to 16 years of age. Journal of the American Academy of Child & Adolescent Psychiatry, 50, 460–470. doi:10.1016/j.jaac.2011.02.001 Google Scholar
Muthen, L. K., & Muthen, M. B. (1998–2009). Mplus: Statistical analyses with latent variables—User's guide. 5.21 ed. Los Angeles: Author.Google Scholar
Nelson, C. A. III, Zeanah, C. H., Fox, N. A., Marshall, P. J., Smyke, A. T., & Guthrie, D. (2007). Cognitive recovery in socially deprived young children: The Bucharest Early Intervention Project. Science, 318, 1937–1940. doi:10.1126/science.1143921 Google Scholar
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics, 3, 97–106.Google Scholar
O'Connor, T. G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biological Psychiatry, 58, 211–217. doi:10.1016/j.biopsych.2005.03.032 Google Scholar
O'Connor, T. G., Bergman, K., Sarkar, P., & Glover, V. (2013). Prenatal cortisol exposure predicts infant cortisol response to acute stress. Developmental Psychobiology, 55, 145–155. doi:10.1002/dev.21007 Google Scholar
O'Connor, T. G., Heron, J., & Glover, V. (2002). Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. Journal of the Americal Academy of Child & Adolescent Psychiatry, 41, 1470–1477.CrossRefGoogle ScholarPubMed
O'Connor, T. G., Heron, J., Golding, J., & Glover, V. (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. Journal of Child Psychology and Psychiatry, 44, 1025–1036.Google Scholar
O'Connor, T. G., Monk, C., & Fitelson, E. M. (2014). Practitioner review: Maternal mood in pregnancy and child development—Implications for child psychology and psychiatry. Journal of Child Psychology and Psychiatry, 55, 99–111.CrossRefGoogle ScholarPubMed
O'Connor, T. G., Winter, M. A., Hunn, J., Carnahan, J., Pressman, E. K., Glover, V., et al. (2013). Prenatal maternal anxiety predicts reduced adaptive immunity in infants. Brain, Behavior, and Immunity, 32, 21–28. doi:10.1016/j.bbi.2013.02.002 Google Scholar
O'Donnell, K. J., Bugge Jensen, A., Freeman, L., Khalife, N., O'Connor, T. G., & Glover, V. (2012). Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology, 37, 818–826. doi:10.1016/j.psyneuen.2011.09.014 Google Scholar
O'Donnell, K. J., Glover, V., Jenkins, J., Browne, D., Ben-Shlomo, Y., Golding, J., et al. (2013). Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology, 38, 1630–1638. doi:10.1016/j.psyneuen.2013.01.008 Google Scholar
Painter, R. C., Roseboom, T. J., & Bleker, O. P. (2005). Prenatal exposure to the Dutch famine and disease in later life: An overview. Reproductive Toxicology, 20, 345–352. doi:10.1016/j.reprotox.2005.04.005 Google Scholar
Ramchandani, P., & Psychogiou, L. (2009). Paternal psychiatric disorders and children's psychosocial development. Lancet, 374, 646–653. doi:10.1016/S0140-6736(09)60238-5 CrossRefGoogle ScholarPubMed
Rice, F., Jones, I., & Thapar, A. (2007). The impact of gestational stress and prenatal growth on emotional problems in offspring: A review. Acta Psychiatric Scandinavia, 115, 171–183. doi: 10.1111/j.1600-0447.2006.00895.x CrossRefGoogle ScholarPubMed
Robinson, M., Mattes, E., Oddy, W. H., Pennell, C. E., van Eekelen, A., McLean, N. J., et al. (2011). Prenatal stress and risk of behavioral morbidity from age 2 to 14 years: The influence of the number, type, and timing of stressful life events. Development and Psychopathology, 23, 507–520. doi:10.1017/S0954579411000241 CrossRefGoogle ScholarPubMed
Satorra, A. (2000). Scaled and adjusted restricted tests in multi-sample analysis of moment structures. In Heijmans, R. D. H., Pollock, D. S. G., & Satorra, A. (Eds.), Innovations in multivariate statistical analysis. A Festschrift for Heinz Neudecker. London: Kluwer Academic.Google Scholar
Scott, S., & O'Connor, T. G. (2012). An experimental test of differential susceptibility to parenting among emotionally-dysregulated children in a randomized controlled trial for oppositional behavior. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 53, 1184–1193. doi:10.1111/j.1469-7610.2012.02586.x Google Scholar
Scott, S., Sylva, K., Doolan, M., Price, J., Jacobs, B., Crook, C., et al. (2010). Randomised controlled trial of parent groups for child antisocial behaviour targeting multiple risk factors: The SPOKES project. Journal of Child Psychology and Psychiatry, 51, 48–57. doi:10.1111/j.1469-7610.2009.02127.x CrossRefGoogle ScholarPubMed
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463.Google Scholar
Stein, A. D., Pierik, F. H., Verrips, G. H., Susser, E. S., & Lumey, L. H. (2009). Maternal exposure to the Dutch famine before conception and during pregnancy: Quality of life and depressive symptoms in adult offspring. Epidemiology, 20, 909–915. doi:10.1097/EDE.0b013e3181b5f227 Google Scholar
van den Bergh, B. R., Mennes, M., Stevens, V., van der Meere, J., Borger, N., Stiers, P., et al. (2006). ADHD deficit as measured in adolescent boys with a continuous performance task is related to antenatal maternal anxiety. Pediatric Research, 59, 78–82. doi:10.1203/01.pdr.0000191143.75673.52 Google Scholar
van den Bergh, B. R., Van Calster, B., Smits, T., Van Huffel, S., & Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 33, 536–545. doi:10.1038/sj.npp.1301450 Google Scholar
Wadhwa, P. D., Buss, C., Entringer, S., & Swanson, J. M. (2009). Developmental origins of health and disease: Brief history of the approach and current focus on epigenetic mechanisms. Seminars in Reproductive Medicine, 27, 358–368. doi:10.1055/s-0029-1237424 Google Scholar
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Table S1

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Table S2

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Table S3

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