Abstract
There is increasing evidence that prenatal stressful life events (SLEs) may be a potential risk factor for attention-deficit hyperactivity disorder (ADHD), but the sex-specific and time-dependent effects of prenatal stress on ADHD are less clear. In this prospective longitudinal study, data on prenatal SLEs during different stages of gestation and indicators of buffers against stress, including maternal social support and avoidance coping, were obtained from 1765 pregnant women at 32 weeks of gestation. The behavioral symptoms of ADHD in children aged 48–54 months were evaluated by reports from the parents. There were 226 children (12.8 %) above the clinically significant cutoff for ADHD. After adjusting for potential confounders, boys whose mother experienced severe SLEs in the second trimester had a significantly increased risk (OR = 2.41, 95 % CI: 1.03–5.66) of developing ADHD symptoms compared with boys whose mothers did not experience severe SLEs at this time. However, no significantly increased risk of ADHD symptoms was observed in girls born to mothers experienced prenatal severe SLEs. Additionally, significant interaction effects of prenatal SLEs, social support and coping style on ADHD symptoms were found in males. Boys whose mothers experienced severe SLEs during the second trimester accompanied by a higher score for avoidance coping (OR = 3.31, 95 % CI: 1.13–9.70) or a lower score for social support (OR = 4.39, 95 % CI: 1.05–18.31) were likely to be at a higher risk for ADHD symptoms. The epidemiological evidence in this prospective follow-up study suggests that the effect of prenatal SLEs on ADHD symptoms in offspring may depend on the timing of prenatal stress and may vary according to the sex of the offspring.
Similar content being viewed by others
Abbreviations
- ADHD:
-
Attention-deficit hyperactivity disorder
- BMI:
-
Body mass index
- PNMS:
-
Prenatal maternal stress
- SLEs:
-
Stressful life events
References
Spencer TJ, Biederman J, Wilens TE, Faraone SV (2002) Overview and neurobiology of attention-deficit/hyperactivity disorder. J Clin Psychiatry 63(Suppl 12):3–9
Hudziak JJ, Derks EM, Althoff RR, Rettew DC, Boomsma DI (2005) The genetic and environmental contributions to attention deficit hyperactivity disorder as measured by the Conners’ Rating Scales-Revised. Am J Psychiatry 162(9):1614–1620. doi:10.1176/appi.ajp.162.9.1614
Owens JA (2005) The ADHD and sleep conundrum: a review. J Dev Behav Pediatr 26(4):312–322
Boyle CA, Boulet S, Schieve LA, Cohen RA, Blumberg SJ, Yeargin-Allsopp M, Visser S, Kogan MD (2011) Trends in the prevalence of developmental disabilities in US children, 1997–2008. Pediatrics 127(6):1034–1042. doi:10.1542/peds.2010-2989
Laplante DP, Barr RG, Brunet A, Galbaud du Fort G, Meaney ML, Saucier JF, Zelazo PR, King S (2004) Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res 56(3):400–410
Kinney DK, Miller AM, Crowley DJ, Huang E, Gerber E (2008) Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J Autism Dev Disord 38(3):481–488. doi:10.1007/s10803-007-0414-0
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. J Psychiatr Res 45(7):879–885. doi:10.1016/j.jpsychires.2010.12.005
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. Eur Child Adolesc Psychiatry 19(10):747–753. doi:10.1007/s00787-010-0113-9
Motlagh MG, Katsovich L, Thompson N, Lin H, Kim YS, Scahill L, Lombroso PJ, King RA, Peterson BS, Leckman JF (2010) Severe psychosocial stress and heavy cigarette smoking during pregnancy: an examination of the pre- and perinatal risk factors associated with ADHD and Tourette syndrome. Eur Child Adolesc Psychiatry 19(10):755–764. doi:10.1007/s00787-010-0115-7
Ronald A, Pennell CE, Whitehouse AJ (2010) Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Front Psychol 1:223. doi:10.3389/fpsyg.2010.00223
Weinstock M (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32(10):1730–1740. doi:10.1007/s11064-007-9339-4
Lobel M, Hamilton JG, Cannella DT (2008) Psychosocial perspectives on pregnancy: prenatal maternal stress and coping. Soc Pers Psychol Compass 2(4):1600–1623
Suenaga T, Yukie M, Gao S, Nakahara D (2012) Sex-specific effects of prenatal stress on neuronal development in the medial prefrontal cortex and the hippocampus. Neuroreport 23(7):430–435. doi:10.1097/WNR.0b013e3283529805
Zhu P, Tao F, Hao J, Sun Y, Jiang X (2010) Prenatal life events stress: implications for preterm birth and infant birthweight. Am J Obstet Gynecol 203(1):34.e31–34.e38. doi:10.1016/j.ajog.2010.02.023
Yang DS, Zhang YL (1990) Behavioral medicine. Hunan Normal University Press, Chagsha
Xiao SY (1994) Theoretical principle and application of social support scale. J Clin Psychiatry 4:98–100
Jiang QJ, Zhu YH (1999) Further explorations for a coping style questionnaire. Chin J Behav Med 8(3):167–169
Conners CK, Barkley RA (1985) Rating scales and checklists for child psychopharmacology. Psychopharmacol Bull 21(4):809–843
Heinonen K, Raikkonen K, Pesonen AK, Andersson S, Kajantie E, Eriksson JG, Vartia T, Wolke D, Lano A (2011) Trajectories of growth and symptoms of attention-deficit/hyperactivity disorder in children: a longitudinal study. BMC Pediatr 11:84. doi:10.1186/1471-2431-11-84
Conners CK, Casat CD, Gualtieri CT, Weller E, Reader M, Reiss A, Weller RA, Khayrallah M, Ascher J (1996) Bupropion hydrochloride in attention deficit disorder with hyperactivity. J Am Acad Child Adolesc Psychiatry 35(10):1314–1321. doi:10.1097/00004583-199610000-00018
zheng W (2010) Epidemiological investigation and treatment effect of attention deficit hyperactivity disorder in child. Chin J Child Health Care 18(04):329–321
Ou P, Cheng X, Qian QF (2001) Diagnostic value of Conners’ Hyperactivity Index in attention deficit hyperactivity disorder. Chin J Child Health Care 9(03):201–203
Zhang F, Wang J, Yin LQ (2003) Application of Conners’ Hyperactivity Index in diagnosis of attention deficit hyperactivity disorder. Chin J Behav Med Sci 12(06):627–630
Daelmans B, Dewey K, Arimond M (2009) New and updated indicators for assessing infant and young child feeding. Food Nutr Bull 30(2 Suppl):S256–S262
Brookhart MA, Schneeweiss S, Rothman KJ, Glynn RJ, Avorn J, Stürmer T (2006) Variable selection for propensity score models. Am J Epidemiol 163(12):1149–1156
Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46(3):246–254. doi:10.1111/j.1469-7610.2004.00359.x
Berger-Sweeney J, Hohmann CF (1997) Behavioral consequences of abnormal cortical development: insights into developmental disabilities. Behav Brain Res 86(2):121–142. doi:10.1016/S0166-4328(96)02251-6
Van den Hove DL, Lauder JM, Scheepens A, Prickaerts J, Blanco CE, Steinbusch HW (2006) Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hippocampus. Brain res 1090(1):29–34. doi:10.1016/j.brainres.2006.03.057
Garcia-Caceres C, Lagunas N, Calmarza-Font I, Azcoitia I, Diz-Chaves Y, Garcia-Segura LM, Baquedano E, Frago LM, Argente J, Chowen JA (2010) Gender differences in the long-term effects of chronic prenatal stress on the HPA axis and hypothalamic structure in rats. Psychoneuroendocrinology 35(10):1525–1535. doi:10.1016/j.psyneuen.2010.05.006
Grigoriadis S, Seeman MV (2002) The role of estrogen in schizophrenia: implications for schizophrenia practice guidelines for women. Can J Psychiatry 47(5):437–442
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 to 9-year-old children. Psychoneuroendocrinology 35(1):141–153. doi:10.1016/j.psyneuen.2009.07.010
Van den Bergh BR, Marcoen A (2004) High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 75(4):1085–1097
Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511–533
Feldman PJ, Dunkel-Schetter C, Sandman CA, Wadhwa PD (2000) Maternal social support predicts birth weight and fetal growth in human pregnancy. Psychosom Med 62(5):715–725
Guardino CM, Dunkel Schetter C (2013) Coping during pregnancy: a systematic review and recommendations. Health Psychol Rev 8(1):70–94. doi:10.1080/17437199.2012.752659
Elsenbruch S, Benson S, Rucke M, Rose M, Dudenhausen J, Pincus-Knackstedt MK, Klapp BF, Arck PC (2007) Social support during pregnancy: effects on maternal depressive symptoms, smoking and pregnancy outcome. Hum Reprod Oxf Engl 22(3):869–877. doi:10.1093/humrep/del432
Dole N, Savitz DA, Siega-Riz AM, Hertz-Picciotto I, McMahon MJ, Buekens P (2004) Psychosocial factors and preterm birth among African American and White women in central North Carolina. Am J Public Health 94(8):1358–1365. doi:10.2105/AJPH.94.8.1358
Acknowledgments
The authors are grateful to the children and the families who participated in this study. This work was supported by National Natural Science Foundation of China (81472991, 81330068, 81373012), National Training Programs of Innovation and Entrepreneurship for Undergraduates (201310366038), Key Project Foundation for the Talents by Educational Commission of Anhui Province (2013SQRL020ZD) and Program for the Innovative Talents of Anhui Medical University.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhu, P., Hao, JH., Tao, RX. et al. Sex-specific and time-dependent effects of prenatal stress on the early behavioral symptoms of ADHD: a longitudinal study in China. Eur Child Adolesc Psychiatry 24, 1139–1147 (2015). https://doi.org/10.1007/s00787-015-0701-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00787-015-0701-9