Abstract
Prenatal maternal stress (PNMS) is linked to physical sequelae in offspring, including childhood asthma. This study sought to examine the roles of objective and subjective PNMS in the development of asthma at offspring ages 5 and 15. The sample included 815 mother–child dyads from the Mater Misericordiae Mothers’ Hospital-University of Queensland Study of Pregnancy. PNMS was measured via retrospective self-report during pregnancy and 3–5 days after birth. Postnatal maternal stress was measured at offspring age 5. Objective PNMS was associated with elevated asthma risk at age 5 (OR 1.21, 95% CI 1.00, 1.45, p = 0.05), albeit not above concurrent postnatal stress. Sex moderated the association between PNMS and asthma at age 15, controlling for postnatal stress. Sex stratified analyses revealed a positive association between objective PNMS and age 15 asthma in females, but not males. Results provide evidence that PNMS may impact asthma outcomes in adolescence.
Similar content being viewed by others
Data Availability
Due to the nature of this research, participants of this study did not agree for their data to be shared publicly, so supporting data is not available.
References
Barker DJ, Osmond C (1989) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1(8489):1077–1081. https://doi.org/10.1016/s0140-6736(86)91340-1
Henderson AJ, Warner JO (2012) Fetal origins of asthma. Semin Fetal Neonatal Med 17(2):82–91. https://doi.org/10.1016/j.siny.2012.01.006
Zacharasiewicz A (2016) Maternal smoking in pregnancy and its influence on childhood asthma. ERJ Open Res 2(3):00042–02016. https://doi.org/10.1183/23120541.00042-201
Baïz N, Just J, Chastang J et al (2019) Maternal diet before and during pregnancy and risk of asthma and allergic rhinitis in children. Allergy Asthma Clin Immunol. https://doi.org/10.1186/s13223-019-0353-2
Darabi B, Rahmati S, HafeziAhmadi MR, Badfar G, Azami M (2019) The association between caesarean section and childhood asthma: an updated systematic review and meta-analysis. Allergy Asthma Clin Immunol 15(1):62. https://doi.org/10.1186/s13223-019-0367-9
Gao Y, Nanan R, Macia L et al (2021) The maternal gut microbiome during pregnancy and offspring allergy and asthma. J Allergy Clin Immunol 148(3):669–678. https://doi.org/10.1016/j.jaci.2021.07.011
O’Connor TG, Sefair AV (2021) Prenatal stress and child health: immune models and mechanisms. In: Wazana A, Székely E, Oberlander TF (eds) Prenatal stress and child development. Springer, Cham, pp 131–163. https://doi.org/10.1007/978-3-030-60159-1_7
Andersson NW, Hansen MV, Larsen AD, Hougaard KS, Kolstad HA, Schlünssen V (2016) Prenatal maternal stress and atopic diseases in the child: a systematic review of observational human studies. Allergy Eur J Allergy Clin Immunol 71(1):15–26. https://doi.org/10.1111/all.12762
Chen S, Chen S (2021) Are prenatal anxiety or depression symptoms associated with asthma or atopic diseases throughout the offspring’s childhood? An updated systematic review and meta-analysis. BMC Pregnancy Childbirth 21(1):435. https://doi.org/10.1186/s12884-021-03909-z
Flanigan C, Sheikh A, Dunn GA, Brew BK, Almqvist C, Nwaru BI (2018) Prenatal psychosocial stress and offspring’s asthma and allergy risk: a systematic review and meta-analysis. Clin Exp Allergy 48(4):403–414. https://doi.org/10.1111/cea.13091
Rosa MJ, Lee A, Wright RJ (2018) Evidence establishing a link between prenatal and early life stress and asthma development. Curr Opin Allergy Clin Immunol 18(2):148–158. https://doi.org/10.1097/ACI.0000000000000421
Turcotte-Tremblay A, Lim R, Laplante DP, Kobzik L, Brunet A, King S (2014) Prenatal maternal stress predicts childhood asthma in girls: project ice storm. BioMed Res Int. https://doi.org/10.1155/2014/201717
Alderdice F, Lynn F, Lobel M (2012) A review and psychometric evaluation of pregnancy-specific stress measures. J Psychosom Obstet Gynecol 33(2):62–77. https://doi.org/10.3109/0167482X.2012.673040
Smith KE, Pollak SD (2020) Early life stress and development: potential mechanisms for adverse outcomes. J Neurodev Disord 12(1):34. https://doi.org/10.1186/s11689-020-09337-y
Pollak SD, Smith KE (2021) Thinking clearly about biology and childhood adversity: next steps for continued progress. Perspect Psychol Sci 16(6):1473–1477. https://doi.org/10.1177/17456916211031539
McLaughlin KA, Sheridan MA, Humphreys KL, Belsky J, Ellis BJ (2021) The value of dimensional models of early experience: thinking clearly about concepts and categories. Perspect Psychol Sci J Assoc Psychol Sci 16(6):1463–1472. https://doi.org/10.1177/1745691621992346
Harkness KL, Monroe SM (2016) The assessment and measurement of adult life stress: basic premises, operational principles, and design requirements. J Abnorm Psychol 125(5):725–745. https://doi.org/10.1037/abn0000178
Van den Bergh BRH, van den Heuvel MI, Lahti M et al (2020) Prenatal developmental origins of behavior and mental health: the influence of maternal stress in pregnancy. Neurosci Biobehav Rev 117:26–64. https://doi.org/10.1016/j.neubiorev.2017.07.003
Tsai CH, Huang JH, Hwang BF, Lee YL (2010) Household environmental tobacco smoke and risks of asthma, wheeze and bronchitic symptoms among children in Taiwan. Respir Res 11(1):11. https://doi.org/10.1186/1465-9921-11-11
Wood BL, Miller BD, Lehman HK (2015) Review of family relational stress and pediatric asthma: the value of biopsychosocial systemic models. Fam Process 54(2):376–389. https://doi.org/10.1111/famp.12139
Lee A, Chiu YM, Rosa MJ et al (2016) Prenatal and postnatal stress and asthma in children: temporal- and sex-specific associations. J Allergy Clin Immunol 138(3):740-747.e3. https://doi.org/10.1016/j.jaci.2016.01.014
Liu X, Olsen J, Agerbo E, Yuan W, Sigsgaard T, Li J (2015) Prenatal stress and childhood asthma in the offspring: role of age at onset. Eur J Public Health 25(6):1042–1046. https://doi.org/10.1093/eurpub/ckv129
Sandman CA, Glynn LM, Davis EP (2013) Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res 75(4):327–335. https://doi.org/10.1016/j.jpsychores.2013.07.009
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179(4068):90–92. https://doi.org/10.1126/science.179.4068.90
Sutherland S, Brunwasser SM (2018) Sex differences in vulnerability to prenatal stress: a review of the recent literature. Curr Psychiatry Rep 20(11):102. https://doi.org/10.1007/s11920-018-0961-4
Glover V, Hill J (2012) Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiol Behav 2012(106):736–740. https://doi.org/10.1016/j.physbeh.2012.02.011
Quarini C, Pearson RM, Stein A, Ramchandani PG, Lewis G, Evans J (2016) Are female children more vulnerable to the long-term effects of maternal depression during pregnancy? J Affect Disord 189:329–335. https://doi.org/10.1016/j.jad.2015.09.039
Shah R, Newcomb DC (2018) Sex bias in asthma prevalence and pathogenesis. Front Immunol 9:2997. https://doi.org/10.3389/fimmu.2018.02997
Balzano G, Fuschillo S, Melillo G, Bonini S (2001) Asthma and sex hormones. Allergy 56(1):13–20. https://doi.org/10.1034/j.1398-9995.2001.00128.x
Asher M, Weiland SK (1998) The International Study of Asthma and Allergies in Childhood (ISAAC) ISAAC Steering Committee. Clin Exp Allergy 28(Suppl 5):52–66. https://doi.org/10.1046/j.1365-2222.1998.028s5052.x
Yung JA, Fuseini H, Newcomb DC (2018) Hormones, sex, and asthma. Ann Allergy Asthma Immunol 120(5):488–494. https://doi.org/10.1016/j.anai.2018.01.016
Fang F, Höglund CO, Arck P et al (2011) Maternal bereavement and childhood asthma-analyses in two large samples of Swedish children. PLoS ONE 6:e27202. https://doi.org/10.1371/journal.pone.0027202
Hsu HH, Chiu YM, Coull BA et al (2015) Prenatal particulate air pollution and asthma onset in urban children. Identifying sensitive windows and sex differences. Am J Respir Crit Care Med 192(9):1052–1059. https://doi.org/10.1164/rccm.201504-0658OC
Lee A, Leon Hsu HH, Mathilda Chiu YH et al (2018) Prenatal fine particulate exposure and early childhood asthma: effect of maternal stress and fetal sex. J Allergy Clin Immunol 141(5):1880–1886. https://doi.org/10.1016/j.jaci.2017.07.017
Hartwig IRV, Bruenahl CA, Ramisch K et al (2014) Reduced levels of maternal progesterone during pregnancy increase the risk for allergic airway diseases in females only. J Mol Med 92:1093–1104. https://doi.org/10.1007/s00109-014-1167-9
Laube M, Thome UH (2022) Y it matters—sex differences in fetal lung development. Biomolecules 12(3):437. https://doi.org/10.3390/biom12030437
Stark MJ, Hodyl NA, Wright IMR, Clifton VL (2011) Influence of sex and glucocorticoid exposure on preterm placental pro-oxidant-antioxidant balance. Placenta 32(11):865–870. https://doi.org/10.1016/j.placenta.2011.08.010
Keeping JD, Najman JM, Morrison J, Western JS, Anderson MJ, Williams GM (1989) A prospective longitudinal study of social, psychological and obstetric factors in pregnancy: response rates and demographic characteristics of the 8556 respondents. BJOG Int J Obstet Gynecol 96(3):289–297. https://doi.org/10.1111/j.1471-0528.1989.tb02388.x
Hammen C, Brennan PA (2001) Depressed adolescents of depressed and nondepressed mothers: tests of an interpersonal impairment hypothesis. J Consult Clin Psychol 69(2):284–294. https://doi.org/10.1037/0022-006X.69.2.284
Reeder LG, Schrama PGM, Dirken JM (1973) Stress and cardiovascular health: an international co-operative study. I Soc Sci Med 7:573–584
Betts KS, Williams GM, Najman JM, Alati R (2014) Maternal depressive, anxious, and stress symptoms during pregnancy predict internalizing problems in adolescence. Depress Anxiety 31:9–18. https://doi.org/10.1002/da.22210
Metcalfe C, Smith GD, Wadsworth E et al (2003) A contemporary validation of the reeder stress inventory. J Health Psychol 8(1):83–94. https://doi.org/10.1348/135910703762879228
Zhang J, Ma C, Yang A, Zhang R, Gong J, Mo F (2018) Is preterm birth associated with asthma among children from birth to 17 years old? -A study based on 2011–2012 US National Survey of Children’s Health. Ital J Pediatr 44(1):151. https://doi.org/10.1186/s13052-018-0583-9
Xu XF, Li YJ, Sheng YJ, Liu JL, Tang LF, Chen ZM (2014) Effect of low birth weight on childhood asthma: a meta-analysis. BMC Pediatr 14:275. https://doi.org/10.1186/1471-2431-14-275
Kozyrskyj AL, Kendall GE, Jacoby P, Sly PD, Zubrick SR (2010) Association between socioeconomic status and the development of asthma: analyses of income trajectories. Am J Public Health 100(3):540–546. https://doi.org/10.2105/AJPH.2008.150771
Lewis KM, Ruiz M, Goldblatt P et al (2017) Mother’s education and offspring asthma risk in 10 European cohort studies. Eur J Epidemiol 32(9):797–805. https://doi.org/10.1007/s10654-017-0309-0
Gauthier TW, Brown LAS (2017) In utero alcohol effects on foetal, neonatal and childhood lung disease. Paediatr Respir Rev 21:34–37. https://doi.org/10.1016/j.prrv.2016.08.006
Brew BK, Lundholm C, Viktorin A, Lichtenstein P, Larsson H, Almqvist C (2018) Longitudinal depression or anxiety in mothers and offspring asthma: a Swedish population-based study. Int J Epidemiol 47(1):166–174. https://doi.org/10.1093/ije/dyx208
Xue M, Dehaas E, Chaudhary N, O’Byrne P, Satia I, Kurmi OP (2021) Breastfeeding and risk of childhood asthma: a systematic review and meta-analysis. ERJ Open Res. https://doi.org/10.1183/23120541.00504-2021
Shepherd CCJ, Li J, Cooper MN, Hopkins KD, Farrant BM (2017) The impact of racial discrimination on the health of Australian Indigenous children aged 5–10 years: analysis of national longitudinal data. Int J Equity Health 16(1):116. https://doi.org/10.1186/s12939-017-0612-0
Melgert BN, Ray A, Hylkema MN, Timens W, Postma DS (2007) Are there reasons why adult asthma is more common in females? Curr Allergy Asthma Rep 7(2):143–150. https://doi.org/10.1007/s11882-007-0012-4
Wright RJ (2010) Perinatal stress and early life programming of lung structure and function. Biol Psychol 84(1):46–56. https://doi.org/10.1016/j.biopsycho.2010.01.007
Veru F, Laplante DP, Luheshi G, King S (2014) Prenatal maternal stress exposure and immune function in the offspring. Stress 17(2):133–148. https://doi.org/10.3109/10253890.2013.876404
Mishra GD, Cooper R, Kuh D (2010) A life course approach to reproductive health: theory and methods. Maturitas 65(2):92–97. https://doi.org/10.1016/j.maturitas.2009.12.009
Mirabelli MC, Beavers SF, Flanders WD, Chatterjee AB (2014) Reliability in reporting asthma history and age at asthma onset. J Asthma Off J Assoc Care Asthma 51(9):956–963. https://doi.org/10.3109/02770903.2014.930480
Acknowledgements
The authors thank the MUSP, M900, and M20 Research Teams and the participating families. We also thank the principal investigators of the Mater-University Study of Pregnancy study, and the Brisbane, Australia staff coordinators.
Funding
This research was supported by NIMH R01MH052239. The authors have no relevant financial or non-financial interests to disclose.
Author information
Authors and Affiliations
Contributions
MRP: Conceptualization, Methodology, Formal Analysis, Writing-Original draft preparation; MLE: Writing-Reviewing and Editing, Supervision; EL: Visualization, Formal Analysis, Writing-Reviewing and Editing; CH: Conceptualization, Resources, Supervision, Funding; PAB: Conceptualization, Methodology, Supervision, Resources, Funding, Writing-Reviewing and Editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
Research Involving Human and Animal Rights
All procedures performed in this study with human participants were in accordance with the ethical standards of the institutional, relevant national guidelines on human experimentation, and with the Helsinki Declaration of 1975, and its later amendments or comparable ethical standards. Specifically, this research protocol was approved by the institutional committees and Internal Review Boards of Emory University, University of Queensland, and UCLA.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pike, M.R., Engel, M.L., Lipner, E. et al. Prenatal Maternal Stress and Pediatric Asthma Across Development: Adolescent Female-Specific Vulnerability. Child Psychiatry Hum Dev (2023). https://doi.org/10.1007/s10578-023-01600-2
Accepted:
Published:
DOI: https://doi.org/10.1007/s10578-023-01600-2