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Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress

Published online by Cambridge University Press:  17 April 2013

Q. A. Class*
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA
K. M. Abel
Affiliation:
Centre for Women's Mental Health, Manchester Academic Health Sciences, University of Manchester, UK
A. S. Khashan
Affiliation:
Anu Research Centre, Department of Obstetrics and Gynaecology, University College Cork, Ireland
M. E. Rickert
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA
C. Dalman
Affiliation:
Department of Public Health Sciences, Division of Public Health Epidemiology, Karolinska Institutet, Stockholm, Sweden
H. Larsson
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
C. M. Hultman
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
N. Långström
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
P. Lichtenstein
Affiliation:
Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
B. M. D‘Onofrio
Affiliation:
Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA
*
*Address for correspondence: Q. A. Class, B.S., Department of Psychological and Brain Sciences, Indiana University, 1101 East 10th St, Bloomington, IN 47405, USA. (Email: qaclass@indiana.edu)

Abstract

Background

Preconception, prenatal and postnatal maternal stress is associated with increased offspring psychopathology, but findings are inconsistent and need replication. We estimated associations between maternal bereavement stress and offspring autism spectrum disorder (ASD), attention deficit hyperactivity disorder (ADHD), bipolar disorder, schizophrenia, suicide attempt and completed suicide.

Method

Using Swedish registers, we conducted the largest population-based study to date examining associations between stress exposure in 738 144 offspring born 1992–2000 for childhood outcomes and 2 155 221 offspring born 1973–1997 for adult outcomes with follow-up to 2009. Maternal stress was defined as death of a first-degree relative during (a) the 6 months before conception, (b) pregnancy or (c) the first two postnatal years. Cox proportional survival analyses were used to obtain hazard ratios (HRs) in unadjusted and adjusted analyses.

Results

Marginal increased risk of bipolar disorder and schizophrenia following preconception bereavement stress was not significant. Third-trimester prenatal stress increased the risk of ASD [adjusted HR (aHR) 1.58, 95% confidence interval (CI) 1.15–2.17] and ADHD (aHR 1.31, 95% CI 1.04–1.66). First postnatal year stress increased the risk of offspring suicide attempt (aHR 1.13, 95% CI 1.02–1.25) and completed suicide (aHR 1.51, 95% CI 1.08–2.11). Bereavement stress during the second postnatal year increased the risk of ASD (aHR 1.30, 95% CI 1.09–1.55).

Conclusions

Further research is needed regarding associations between preconception stress and psychopathological outcomes. Prenatal bereavement stress increases the risk of offspring ASD and ADHD. Postnatal bereavement stress moderately increases the risk of offspring suicide attempt, completed suicide and ASD. Smaller previous studies may have overestimated associations between early stress and psychopathological outcomes.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2013 

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References

Abel, KM, Wicks, S, Susser, ES, Dalman, C, Pedersen, MG, Mortensen, PB, Webb, RT (2010). Birth weight, schizophrenia, and adult mental disorder. Archives of General Psychiatry 67, 923930.CrossRefGoogle ScholarPubMed
Academy of Medical Sciences Working Group (2007). Identifying the environmental causes of disease: how should we decide what to believe and when to take action? Academy of Medical Sciences: London.Google Scholar
Arbuckle, NW, de Vries, B (1995). The long-term effects of later life spousal and parental bereavement on personal functioning. The Gerontologist 35, 637647.Google Scholar
Bagner, DM, Pettit, JW, Lewinsohn, PM, Seeley, JR (2010). Effect of maternal depression on child behavior: a sensitive period? Journal of the American Academy of Child and Adolescent Psychiatry 49, 699707.Google Scholar
Bailey, A, Luthert, P, Dean, A, Harding, B, Janota, I, Montgomery, M, Rutter, M, Lantos, P (1998). A clinicopathological study of autism. Brain 121, 889905.Google Scholar
Bale, TL, Baram, TZ, Brown, AS, Goldstein, JM, Insel, TR, McCarthy, MM, Nemeroff, CB, Reyes, TM, Simerly, RB, Susser, ES, Nestler, EJ (2010). Early life programming and neurodevelopmental disorders. Biological Psychiatry 68, 314319.CrossRefGoogle ScholarPubMed
Barker, DJP (1998). Mothers, Babies and Health in Later Life. Churchill Livingstone: Edinburgh.Google Scholar
Bauman, ML, Kemper, TL (1994). Neuroanatomic observations of the brain in autism. In The Neurobiology of Autism (ed. Bauman, M. L. and Kemper, T. L.), pp. 119145. John Hopkins University Press: Baltimore.Google Scholar
Bauman, ML, Kemper, TL (2005). Neuroanatomic observations of the brain in autism: a review and future directions. International Journal of Developmental Neuroscience 23, 183187.Google Scholar
Beversdorf, DQ, Manning, SE, Hillier, A, Anderson, SL, Nordgren, RE, Walters, SE, Nagaraja, HN, Cooley, WC, Gaelic, SE, Bauman, ML (2005). Timing of prenatal stressors and autism. Journal of Autism and Developmental Disorders 35, 471478.Google Scholar
Beydoun, H, Saftlas, AF (2008). Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatric and Perinatal Epidemiology 22, 438466.CrossRefGoogle ScholarPubMed
Brand, SR, Engel, SM, Canfield, RL, Yehuda, R (2006). The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Annals of the New York Academy of Sciences 1071, 454458.Google Scholar
Brent, DA, Mann, JJ (2005). Family genetic studies, suicide, and suicidal behavior. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 133C, 1324.CrossRefGoogle ScholarPubMed
Brent, DA, Mann, JJ (2006). Familial pathways to suicidal behavior: understanding and preventing suicide among adolescents. New England Journal of Medicine 355, 27192721.CrossRefGoogle ScholarPubMed
Brown, AS, Susser, ES, Lin, SP, Neugebauer, R, Gorman, JM (1995). Increased risk of affective disorder in males after second trimester prenatal exposure to the Dutch hunger winter of 1944–1945. British Journal of Psychiatry 166, 601606.Google Scholar
Brown, AS, van Os, J, Driessens, C, Hoek, HW, Susser, ES (2000). Further evidence of relation between prenatal famine and major affective disorder. American Journal of Psychiatry 157, 190195.CrossRefGoogle ScholarPubMed
Buss, C, Davis, EP, Muftuler, LT, Head, K, Sandman, CA (2010). High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology 35, 141153.CrossRefGoogle ScholarPubMed
Buss, C, Davis, EP, Shahbaba, B, Pruessner, JC, Head, K, Sandman, CA (2012). Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proceedings of the National Academy of Sciences USA 109, E1312E1319.Google Scholar
Caspi, A, Moffitt, TE, Newman, DL, Silva, PA (1996). Behavioural observations at age 3 years predicts psychiatric disorders: longitudinal evidence from a birth cohort. Archives of General Psychiatry 53, 10331039.Google Scholar
Centre for Epidemiology (2003). The Swedish Medical Birth Register – a summary of content and quality. (http://www.socialstyrelsen.se/Lists/Artikelkatalog/Attachments/10655/2003-112-3_20031123.pdf).Google Scholar
Charil, A, Laplante, DP, Vaillancourt, C, King, S (2010). Prenatal stress and brain development. Brain Research Reviews 65, 5679.CrossRefGoogle ScholarPubMed
Class, QA, Lichtenstein, P, Langstrom, N, D'Onofrio, BM (2011). Timing of prenatal maternal severe life events and adverse pregnancy outcomes: a population study of 2.6 million pregnancies. Psychosomatic Medicine 73, 234241.CrossRefGoogle ScholarPubMed
Cnattingius, S, Ericson, A, Gunnarskog, J, Kallen, B (1990). A quality study of a medical birth registry. Scandinavian Journal of Social Medicine 18, 105109.Google Scholar
Dunkel-Schetter, C, Glynn, L (2011). Stress in pregnancy: empirical evidence and theoretical issues to guide interdisciplinary research. In Handbook of Stress (ed. Contrada, R. and Baum, A.), pp. 321343. New York, NY: Springer Publishing Company.Google Scholar
Epstein, T, Saltzman-Benaiah, J, O'Hare, A, Goll, JC, Tuck, S (2008). Associated features of Asperger Syndrome and their relationship to parenting stress. Child: Care, Health and Development 34, 503511.CrossRefGoogle ScholarPubMed
Fazel, S, Grann, M (2006). The population impact of severe mental illness on violent crime. American Journal of Psychiatry 163, 13971403.CrossRefGoogle ScholarPubMed
Ganz, ML (2007). The lifetime distribution of the incremental societal costs of autism. Archives of Pediatric Adolescent Medicine 161, 343349.Google Scholar
Gluckman, PD, Hanson, MA (2004). Living with the past: evolution, development, and patterns of disease. Science 305, 17331736.Google Scholar
Glynn, L, Wadhwa, PD, Schetter, CD, Chicz-Demet, A, Sandman, CA (2001). When stress happens matters: effects of earthquake timing on stress responsivity in pregnancy. American Journal of Obstetrics and Gynecology 184, 637642.CrossRefGoogle ScholarPubMed
Goodman, SH, Gotlib, IH (1999). Risk for psychopathology in the children of depressed mothers: a developmental model for understanding mechanisms of transmission. Psychological Review 106, 458490.Google Scholar
Guinchat, V, Thorsen, P, Laurent, C, Cans, C, Bodeau, N, Cohen, D (2012). Pre-, peri- and neonatal risk factors for autism. Acta Obstetrica Gynecologica Scandinavica 91, 287300.Google Scholar
Heim, C, Newport, DJ, Mletzko, T, Miller, AH, Nemeroff, CB (2008). The link between childhood truama and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33, 693710.Google Scholar
Hultman, CM, Torrang, A, Tuvblad, C, Cnattingius, S, Larsson, J, Lichtenstein, P (2007). Birth weight and attention-deficit/hyperactivity symptoms in childhood and early adolescence: a prospective Swedish twin study. Journal of the American Academy of Child and Adolescent Psychiatry 46, 370377.CrossRefGoogle ScholarPubMed
Huttunen, M, Niskanen, P (1978). Prenatal loss of father and psychiatric disorders. Archives of General Psychiatry 35, 429431.Google Scholar
Jablensky, A (2000). Epidemiology of schizophrenia: the global burden of disease and disability. European Archives of Psychiatry and Clinical Neuroscience 250, 274285.Google Scholar
Jirtle, RL, Skinner, MK (2007). Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8, 253262.Google Scholar
Khashan, AS, Abel, KM, McNamee, R, Pedersen, MG, Webb, RT, Baker, PN, Kenny, LC, Mortensen, PB (2008 a). Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Archives of General Psychiatry 65, 146152.Google Scholar
Khashan, AS, McNamee, R, Abel, KM, Mortensen, PB, Kenny, LC, Pedersen, MG, Webb, RT, Baker, PN (2009). Rates of preterm birth following antenatal maternal exposure to severe life events: a population-based cohort study. Human Reproduction 24, 429437.Google Scholar
Khashan, AS, McNamee, R, Abel, KM, Pedersen, MG, Webb, RT, Kenny, LC, Mortensen, PB, Baker, PN (2008 b). Reduced infant birthweight consequent upon maternal exposure to severe life events. Psychosomatic Medicine 70, 688694.Google Scholar
Khashan, AS, McNamee, R, Henriksen, TB, Pedersen, MG, Kenny, LC, Abel, KM, Mortensen, PB (2011). Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. Journal of Psychiatric Research 45, 879885.Google Scholar
King, S, Laplante, DP (2005). The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm. Stress 8, 3545.CrossRefGoogle ScholarPubMed
Kinney, DK, Miller, AM, Crowley, DJ, Huang, E, Gerber, E (2008 a). Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. Journal of Autism and Developmental Disorders 38, 481488.CrossRefGoogle ScholarPubMed
Kinney, DK, Munir, K, Crowley, DJ, Miller, AM (2008 b). Prenatal stress and risk for autism. Neuroscience and Biobehavioral Reviews 32, 15191532.Google Scholar
Landau, R, Avital, M, Berger, A, Atzaba-Poria, N, Arbelle, S, Faroy, M, Auerbach, JG (2010). Parenting of 7-month-old infants at familial risk for attention deficit/hyperactivity disorder. Infant Mental Health Journal 31, 141158.CrossRefGoogle ScholarPubMed
Li, J, Olsen, J, Vestergaard, M, Obel, C (2010). Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. European Child and Adolescent Psychiatry 19, 747753.CrossRefGoogle ScholarPubMed
Li, J, Vestergaard, M, Obel, C, Christensen, J, Precht, DH, Lu, M, Olsen, J (2009). A nationwide study on the risk of autism after prenatal stress exposure to maternal bereavement. Pediatrics 123, 11021107.Google Scholar
Lichtenstein, P, Yip, BH, Bjork, C, Pawitan, Y, Cannon, T, Sullivan, PF, Hultman, CM (2009). Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373, 234239.Google Scholar
Lindstrom, K, Lindblad, F, Hjern, A (2009). Psychiatric morbidity in adolescents and young adults born preterm: a Swedish national cohort study. Pediatrics 123, e47e53.Google Scholar
Lindstrom, K, Lindblad, F, Hjern, A (2011). Preterm birth and attention-deficit/hyperactivity disorder in schoolchildren. Pediatrics 127, 858865.Google Scholar
Liu, J, Dietz, K, Deloyht, JM, Pedre, X, Kelkar, D, Kaur, J, Vialou, V, Lobo, MK, Dietz, DM, Nestler, EJ, Dupree, J, Casaccia, P (2012). Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nature Neuroscience 15, 16211623.Google Scholar
Losh, M, Esserman, D, Anckarsater, H, Sullivan, PF, Lichtenstein, P (2011). Lower birth weight indicates higher risk of autistic traits in discordant twin pairs. Psychological Medicine 42, 10911102.Google Scholar
Mann, JJ (2003). Neurobiology of suicidal behavior. Nature Reviews Neuroscience 4, 819828.Google Scholar
Mantymaa, M, Puura, K, Luoma, I, Latva, R, Salmelin, RK, Tamminen, T (2012). Predicting internalizing and externalizing problems at five years by child and parental factors in infancy and toddlerhood. Child Psychiatry and Human Development 43, 153170.Google Scholar
Matthews, KA, Rodin, J (1992). Pregnancy alters blood pressure responses to psychological and physical challenge. Psychophysiology 29, 232240.CrossRefGoogle ScholarPubMed
Meaney, MJ (2010). Epigenetics and the biological definition of gene × environment interactions. Child Development 81, 4179.Google Scholar
Mittendorfer-Rutz, E, Rasmussen, F, Wasserman, D (2004). Restricted fetal growth and adverse maternal psychosocial and socioeconomic conditions as risk factors for suicidal behavior of offspring: a cohort study. Lancet 364, 11351140.Google Scholar
Monk, C, Georgieff, MK, Osterholm, EA (2013). Research review: maternal prenatal distress and poor nutrition – mutually influencing risk factors affecting infant neurocognitive development. Journal of Child Psychology and Psychiatry, and Allied Disciplines 54, 115130.Google Scholar
Mortensen, PB, Pedersen, CB, Melbye, M, Mors, O, Ewald, H (2003). Individual and familial risk factors for bipolar affective disorders in Denmark. Archives of General Psychiatry 60, 12091215.Google Scholar
Moster, D, Lie, RT, Markestad, T (2008). Long-term medical and social consequences of preterm birth. New England Journal of Medicine 359, 262273.CrossRefGoogle ScholarPubMed
O'Connor, TG, Heron, J, Golding, J, Glover, V; ALSPAC Study Team (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. Journal of Child Psychology and Psychiatry 44, 10251036.Google Scholar
Pelham, WE, Foster, EM, Robb, JA (2007). The economic impact of attention-deficit/hyperactivity disorder in children and adolescents. Journal of Pediatric Psychology 32, 711727.Google Scholar
Piven, J, Palmer, P (1999). Psychiatric disorder and the broad autism phenotype: evidence from a family study of multiple-incidence autism families. American Journal of Psychiatry 156, 557563.CrossRefGoogle ScholarPubMed
Polanczyk, G, De Lima, MS, Horta, BL, Biederman, J, Rohde, LA (2007). The worldwide prevalence of ADHD: a systematic review and metaregression analysis. American Journal of Psychiatry 164, 942948.Google Scholar
Rai, D, Golding, J, Magnusson, C, Steer, C, Lewis, G, Dalman, C (2012). Prenatal and early life exposure to stressful life events and risk of autism spectrum disorders: population-based studies in Sweden and England. PLoS One 7, e38893.Google Scholar
Rice, F, Harold, GT, Boivin, J, van den Bree, M, Hay, DF, Thapar, A (2010). The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychological Medicine 40, 335345.Google Scholar
Rodriguez, A, Bohlin, G (2005). Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? Journal of Child Psychology and Psychiatry 46, 246254.Google Scholar
Ronald, A, Pennell, CE, Whitehouse, AJO (2011). Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Frontiers in Developmental Psychology 1, 223.Google Scholar
Rosenberg, SD, Weili, L, Mueser, KT, Jankowski, MK, Cournos, F (2007). Correlates of adverse childhood events among adults with schizophrenia spectrum disorders. Psychiatric Services 58, 245253.CrossRefGoogle ScholarPubMed
Rutter, M (2007). Proceeding from observed correlation to causal inference: the use of natural experiments. Perspectives on Psychological Science 2, 377395.CrossRefGoogle ScholarPubMed
Rutter, M, Kim-Cohen, J, Maughan, B (2006). Continuities and discontinuities in psychopathology between childhood and adulthood. Journal of Child Psychology and Psychiatry 47, 276295.Google Scholar
Schelar, E, Franzetta, K, Manlove, J (2007). Repeat Teen Childbearing: Differences Across States and by Race and Ethnicity. Research Brief. Child Trends: Washington, DC.Google Scholar
Schulz, R, Mendelsohn, AB, Haley, WE, Mahoney, D, Allen, RS, Zhang, S, Thompson, L, Belle, SH, Resources for Enhancing Alzheimer's Caregiver Health Investigators (2003). End-of-life care and the effects of bereavement on family caregivers of persons with dementia. New England Journal of Medicine 349, 19361942.Google Scholar
Selten, JP, Cantor-Graae, E, Nahon, D, Levav, I, Aleman, A, Kahn, RS (2003). No relationship between risk of schiophrenia and prenatal exposure to stress during the Six-Day War or Yom Kippur War in Israel. Schizophrenia Research 63, 131135.Google Scholar
Shachar-Dadon, A, Schulkin, J, Leshem, M (2009). Adversity before conception will affect adult progeny in rats. Developmental Psychology 45, 916.CrossRefGoogle ScholarPubMed
Simonoff, E, Pickles, A, Charman, T, Chandler, S, Loucas, T, Baird, G (2008). Psychiatric disorders in children with autism spectrum disorders: prevalence, comorbidity, and associated factors in a population-derived sample. Journal of the American Academy of Child and Adolescent Psychiatry 47, 921929.CrossRefGoogle Scholar
Smith, GCS, Pell, JP, Dobbie, R (2003). Interpregnancy interval and risk of preterm birth and neonatal death: retrospective cohort study. British Medical Journal 327, 313.Google Scholar
Smith, GD (2008). Assessing intrauterine influences on offspring health outcomes: can epidemiological studies yield robust findings? Basic and Clinical Pharmacology and Toxicology 102, 245256.Google Scholar
Smits, L, Essed, GGM (2001). Short interpregnancy intervals and unfavourable pregnancy outcome: role of folate depletion. Lancet 358, 20742077.Google Scholar
StClair, D, Xu, M, Wang, P, Yu, Y, Fang, Y, Zhang, F, Zheng, X, Gu, N, Feng, G, Sham, P, He, L (2005). Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959–1961. Journal of the American Medical Association 294, 557562.Google Scholar
Statistics Sweden (2006). Multi-Generation Register 2005. A Description of Contents and Quality. Statistics Sweden: Orebro.Google Scholar
Statistics Sweden (2011). Educational Attainment of the Population (http://www.scb.se/Pages/SubjectArea_3930.aspx). Accessed 1 November 2011.Google Scholar
Talge, NM, Neal, C, Glover, V (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? Journal of Child Psychology and Psychiatry 48, 245261.Google Scholar
Tidemalm, D, Langstrom, N, Lichtenstein, P, Runeson, B (2008). Risk of suicide after suicide attempt according to coexisting psychiatric disorder: Swedish cohort study with long term follow-up. British Medical Journal 337, a2205.Google Scholar
Van den Bergh, BR, Mulder, EJ, Mennes, M, Glover, V (2005). Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neuroscience and Biobehavioral Reviews 29, 237258.Google Scholar
Van den Bergh, BR, Van Calster, BV, 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, 536545.CrossRefGoogle ScholarPubMed
van Os, J, Selten, JP (1998). Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of the Netherlands. British Journal of Psychiatry 172, 324326.Google Scholar
Wadhwa, PD (2005). Psychoneuroendocrine processes in human pregnancy influence fetal development and health. Psychoneuroendocrinology 30, 724743.Google Scholar
Ward, AJ (1990). A comparison and analysis of the presence of family problems during pregnancy of mothers of ‘autistic’ children and mothers of typically developing children. Child Psychiatry and Human Development 20, 279288.Google Scholar
Whiffen, VE, Gotlib, IH (1989). Infants of postpartum depressed mothers: temperament and cognitive status. Journal of Abnormal Psychology 98, 274279.Google Scholar
Williams, JMG, Pollock, LR (2000). The psychology of suicidal behavior. In International Handbook of Suicide and Attempted Suicide (ed. Hawton, K. and Heeringen, K. V.), pp. 7993. Wiley: Chichester.Google Scholar