Abstract
Background
The COVID-19 pandemic dramatically altered the psychosocial environment of pregnant women and new mothers. In addition, prenatal infection is a known risk factor for altered fetal development. Here we examine joint effects of maternal psychosocial stress and COVID-19 infection during pregnancy on infant attention at 6 months postpartum.
Method
One-hundred and sixty-seven pregnant mothers and infants (40% non-White; n = 71 females) were recruited in New York City (n = 50 COVID+, n = 117 COVID–). Infants’ attentional processing was assessed at 6 months, and socioemotional function and neurodevelopmental risk were evaluated at 12 months.
Results
Maternal psychosocial stress and COVID-19 infection during pregnancy jointly predicted infant attention at 6 months. In mothers reporting positive COVID-19 infection, higher prenatal psychosocial stress was associated with lower infant attention at 6 months. Exploratory analyses indicated that infant attention in turn predicted socioemotional function and neurodevelopmental risk at 12 months.
Conclusions
These data suggest that maternal psychosocial stress and COVID-19 infection during pregnancy may have joint effects on infant attention at 6 months. This work adds to a growing literature on the effects of the COVID-19 pandemic on infant development, and may point to maternal psychosocial stress as an important target for intervention.
Impact
-
This study found that elevated maternal psychosocial stress and COVID-19 infection during pregnancy jointly predicted lower infant attention scores at 6 months, which is a known marker of risk for neurodevelopmental disorder. In turn, infant attention predicted socioemotional function and risk for neurodevelopmental disorder at 12 months. These data suggest that maternal psychosocial stress may modulate the effects of gestational infection on neurodevelopment and highlight malleable targets for intervention.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 14 print issues and online access
$259.00 per year
only $18.50 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The data analyzed in the current study are available from the corresponding author upon reasonable request.
References
Glover, V. Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J. Child Psychol. Psychiatry 52, 356–367 (2011).
Morey, J. N., Boggero, I. A., Scott, A. B. & Segerstrom, S. C. Current directions in stress and human immune function. Curr. Opin. Psychol. 5, 13–17 (2015).
Gouin, J.-P. & Kiecolt-Glaser, J. K. The impact of psychological stress on wound healing: methods and mechanisms. Immunol. Allergy Clin. North Am. 31, 81–93 (2011).
Kristenson, M., Eriksen, H. R., Sluiter, J. K., Starke, D. & Ursin, H. Psychobiological mechanisms of socioeconomic differences in health. Soc. Sci. Med. 58, 1511–1522 (2004).
Johnson, M. H., Gliga, T., Jones, E. & Charman, T. Annual research review: infant development, autism, and ADHD – early pathways to emerging disorders. J. Child Psychol. Psychiatry 56, 228–247 (2015).
Brandes-Aitken, A., Braren, S., Swingler, M., Voegtline, K. & Blair, C. Sustained attention in infancy: a foundation for the development of multiple aspects of self-regulation for children in poverty. J. Exp. Child Psychol. 184, 192–209 (2019).
Hendry, A., Johnson, M. H. & Holmboe, K. Early development of visual attention: change, stability, and longitudinal associations. Annu. Rev. Dev. Psychol. 1, 251–275 (2019).
Madigan, S. et al. A meta-analysis of maternal prenatal depression and anxiety on child socioemotional development. J. Am. Acad. Child Adolesc. Psychiatry 57, 645–657.e8 (2018).
Manzari, N., Matvienko-Sikar, K., Baldoni, F., O’Keeffe, G. W. & Khashan, A. S. Prenatal maternal stress and risk of neurodevelopmental disorders in the offspring: a systematic review and meta-analysis. Soc. Psychiatry Psychiatr. Epidemiol. 54, 1299–1309 (2019).
Lafortune, S. et al. Effect of natural disaster-related prenatal maternal stress on child development and health: a meta-analytic review. Int. J. Environ. Res. Public Health 18, 8332 (2021).
Anderson, P. J. & Burnett, A. Assessing developmental delay in early childhood—concerns with the Bayley-III scales. Clin. Neuropsychol. 31, 371–381 (2017).
Muthusamy, S., Wagh, D., Tan, J., Bulsara, M. & Rao, S. Utility of the ages and stages questionnaire to identify developmental delay in children aged 12 to 60 months. JAMA Pediatr. 176, 980 (2022).
Amso, D. & Scerif, G. The attentive brain: insights from developmental cognitive neuroscience. Nat. Rev. Neurosci. 16, 606–619 (2015).
Oakes, L. M. & Amso, D. Development of visual attention. in Stevens’ Handbook of Experimental Psychology and Cognitive Neuroscience (ed. Wixted, J. T.) 1–33 (John Wiley & Sons). https://doi.org/10.1002/9781119170174.epcn401 (2018).
Posner, M. I., Rothbart, M. K., Sheese, B. E. & Voelker, P. Developing attention: behavioral and brain mechanisms. Adv. Neurosci. 2014, 1–9 (2014).
Rueda, M. R. & Posner, M. I. Development of attention networks. in The Oxford Handbook of Developmental Psychology, Vol. 1 (ed. Zelazo, P. D.) 682–705 (Oxford University Press). https://doi.org/10.1093/oxfordhb/9780199958450.013.0024 (2013).
Ungerleider, L. ‘What’ and ‘where’ in the human brain. Curr. Opin. Neurobiol. 4, 157–165 (1994).
van Essen, D. C. & Maunsell, J. H. R. Hierarchical organization and functional streams in the visual cortex. Trends Neurosci. 6, 370–375 (1983).
Rose, S. A., Feldman, J. F. & Jankowski, J. J. Implications of infant cognition for executive functions at age 11. Psychol. Sci. 23, 1345–1355 (2012).
Cuevas, K. & Bell, M. A. Infant attention and early childhood executive function. Child Dev. 85, 397–404 (2014).
Johnson, M. H., Posner, M. I. & Rothbart, M. K. Components of visual orienting in early infancy: contingency learning, anticipatory looking, and disengaging. J. Cogn. Neurosci. 3, 335–344 (1991).
Papageorgiou, K. A. et al. Individual differences in infant fixation duration relate to attention and behavioral control in childhood. Psychol. Sci. 25, 1371–1379 (2014).
Miller, M., Iosif, A.-M., Young, G. S., Hill, M. M. & Ozonoff, S. Early detection of ADHD: insights from infant siblings of children with autism. J. Clin. Child Adolesc. Psychol. 47, 737–744 (2018).
Pérez-Edgar, K. Attention mechanisms in behavioral inhibition: exploring and exploiting the environment. in Behavioral Inhibition 237–261 (Springer International Publishing). https://doi.org/10.1007/978-3-319-98077-5_11 (2018).
Tau, G. Z. & Peterson, B. S. Normal development of brain circuits. Neuropsychopharmacology 35, 147–168 (2010).
Plamondon, A. et al. Spatial working memory and attention skills are predicted by maternal stress during pregnancy. Early Hum. Dev. 91, 23–29 (2015).
Ronald, A., Pennell, C. E. & Whitehouse, A. J. O. Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Front. Psychol. 1, 223 (2011).
Merced‐Nieves, F. M., Dzwilewski, K. L. C., Aguiar, A., Lin, J. & Schantz, S. L. Associations of prenatal maternal stress with measures of cognition in 7.5‐month‐old infants. Dev. Psychobiol. 63, 960–972 (2021).
Tu, H.-F., Skalkidou, A., Lindskog, M. & Gredebäck, G. Maternal childhood trauma and perinatal distress are related to infants’ focused attention from 6 to 18 months. Sci. Rep. 11, 24190 (2021).
Beijers, R., Buitelaar, J. K. & de Weerth, C. Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis. Eur. Child Adolesc. Psychiatry 23, 943–956 (2014).
Hantsoo, L., Kornfield, S., Anguera, M. C. & Epperson, C. N. Inflammation: a proposed intermediary between maternal stress and offspring neuropsychiatric risk. Biol. Psychiatry 85, 97–106 (2019).
Mazza, M. G. et al. Anxiety and depression in COVID-19 survivors: Role of inflammatory and clinical predictors. Brain Behav. Immun. 89, 594–600 (2020).
Thomason, M. E., Werchan, D. & Hendrix, C. L. COVID-19 patient accounts of illness severity, treatments and lasting symptoms. Sci. Data 9, 2 (2022).
Thomason, M. E., Hendrix, C. L., Werchan, D. & Brito, N. H. Perceived discrimination as a modifier of health, disease, and medicine: empirical data from the COVID-19 pandemic. Transl. Psychiatry 12, 284 (2022).
Taquet, M., Luciano, S., Geddes, J. R. & Harrison, P. J. Bidirectional associations between COVID-19 and psychiatric disorder: retrospective cohort studies of 62 354 COVID-19 cases in the USA. Lancet Psychiatry 8, 130–140 (2021).
Boldrini, M., Canoll, P. D. & Klein, R. S. How COVID-19 affects the brain. JAMA Psychiatry 78, 682 (2021).
Iadecola, C., Anrather, J. & Kamel, H. Effects of COVID-19 on the nervous system. Cell 183, 16–27.e1 (2020).
Mukerji, S. S. & Solomon, I. H. What can we learn from brain autopsies in COVID-19? Neurosci. Lett. 742, 135528 (2021).
Beurel, E., Toups, M. & Nemeroff, C. B. The bidirectional relationship of depression and inflammation: double trouble. Neuron 107, 234–256 (2020).
Provenzi, L. et al. Prenatal maternal stress during the COVID-19 pandemic and infant regulatory capacity at 3 months: a longitudinal study. Dev. Psychopathol. 35, 35–43. https://doi.org/10.1017/S0954579421000766 (2023).
Bianco, C. et al. Pandemic beyond the virus: maternal COVID-related postnatal stress is associated with infant temperament. Pediatr. Res. 93, 253–259 (2023).
Fiske, A., Scerif, G. & Holmboe, K. Maternal depressive symptoms and early childhood temperament before and during the COVID‐19 pandemic in the United Kingdom. Infant Child Dev. 31, e2354 (2022).
Sperber, J. F., Hart, E. R., Troller‐Renfree, S. V., Watts, T. W. & Noble, K. G. The effect of the COVID‐19 pandemic on infant development and maternal mental health in the first 2 years of life. Infancy 28, 107–135 (2023).
Shuffrey, L. C. et al. Association of birth during the COVID-19 pandemic with neurodevelopmental status at 6 months in infants with and without in utero exposure to maternal SARS-CoV-2 infection. JAMA Pediatr. 176, e215563 (2022).
Werchan, D. M. et al. Behavioral coping phenotypes and associated psychosocial outcomes of pregnant and postpartum women during the COVID-19 pandemic. Sci. Rep. 12, 1209 (2022).
Hendrix, C. L. et al. Geotemporal analysis of perinatal care changes and maternal mental health: an example from the COVID-19 pandemic. Arch. Womens Ment. Health 25, 943–956 (2022).
Thomason, M. E., Graham, A. & VanTieghem, M. R. The COPE-IS: Coronavirus Perinatal Experiences–Impact Survey (2020). COVGEN. https://www.covgen.org/cope-surveys
Kraybill, J. H., Kim-Spoon, J. & Bell, M. A. Infant attention and age 3 executive function. Yale J. Bio. Med. 92, 3–11 (2019).
Gustafsson, H. C. et al. Innovative methods for remote assessment of neurobehavioral development. Dev. Cogn. Neurosci. 52, 101015 (2021).
Werchan, D. M., Thomason, M. E. & Brito, N. H. OWLET: an automated, open-source method for infant gaze tracking using smartphone and webcam recordings. Behav. Res. Methods 1–15. https://doi.org/10.3758/s13428-022-01962-w (2022).
Derogatis, L. R. BSI 18, Brief Symptom Inventory 18: Administration, Scoring and Procedures Manual (NCS Pearson, Incorporated., 2001).
Blevins, C. A., Weathers, F. W., Davis, M. T., Witte, T. K. & Domino, J. L. The Posttraumatic Stress Disorder Checklist for DSM-5 (PCL-5): development and initial psychometric evaluation. J. Trauma Stress 28, 489–498 (2015).
Jankowski, J. J., Rose, S. A. & Feldman, J. F. Modifying the distribution of attention in infants. Child Dev. 72, 339–351 (2001).
Colombo, J., Mitchell, D. W., Coldren, J. T. & Freeseman, L. J. Individual differences in infant visual attention: are short lookers faster processors or feature processors? Child Dev. 62, 1247–1257 (1991).
Hou, X. & Zhang, L. Saliency detection: a spectral residual approach. in 2007 IEEE Conference on Computer Vision and Pattern Recognition 1–8 (IEEE). https://doi.org/10.1109/CVPR.2007.383267 (2007).
Itti, L. & Koch, C. A saliency-based search mechanism for overt and covert shifts of visual attention. Vis. Res. 40, 1489–1506 (2000).
Gartstein, M. A. & Rothbart, M. K. Studying infant temperament via the Revised Infant Behavior Questionnaire. Infant Behav. Dev. 26, 64–86 (2003).
Rothbart, M. K., Derryberry, D. & Hershey, K. Stability of temperament in childhood: laboratory infant assessment to parent report at seven years. in Temperament and Personality Development Across the Life Span 85–119 (Lawrence Erlbaum Associates Publishers, 2000).
Colombo, J. & Cheatham, C. L. The emergence and basis of endogenous attention in infancy and early childhood. Adv. Child Dev. Behav. 34, 283–322. https://doi.org/10.1016/S0065-2407(06)80010-8 (2006).
Hendry, A. et al. Developmental change in look durations predicts later effortful control in toddlers at familial risk for ASD. J. Neurodev. Disord. 10, 3 (2018).
Gartstein, M. A., Bridgett, D. J., Young, B. N., Panksepp, J. & Power, T. Origins of effortful control: infant and parent contributions. Infancy 18, 149–183 (2013).
Carter, A. S., Briggs-Gowan, M. J., Jones, S. M. & Little, T. D. The Infant-Toddler Social and Emotional Assessment (ITSEA): factor structure, reliability, and validity. J. Abnorm. Child Psychol. 31, 495–514 (2003).
Karabekiroglu, K., Briggs-Gowan, M. J., Carter, A. S., Rodopman-Arman, A. & Akbas, S. The clinical validity and reliability of the Brief Infant–Toddler Social and Emotional Assessment (BITSEA). Infant Behav. Dev. 33, 503–509 (2010).
Cox, J. L., Holden, J. M. & Sagovsky, R. Detection of postnatal depression. Br. J. Psychiatry 150, 782–786 (1987).
Werchan, D. M., Lynn, A., Kirkham, N. Z. & Amso, D. The emergence of object‐based visual attention in infancy: a role for family socioeconomic status and competing visual features. Infancy 24, 752–767. https://doi.org/10.1111/infa.12309 (2019).
Peugh, J. L. & Enders, C. K. Missing data in educational research: a review of reporting practices and suggestions for improvement. Rev. Educ. Res. 74, 525–556 (2004).
Welch, M. G. Calming cycle theory: the role of visceral/autonomic learning in early mother and infant/child behaviour and development. Acta Paediatrica 105, 1266–1274. https://doi.org/10.1111/apa.13547 (2016).
Belsky, J. & van IJzendoorn, M. H. Genetic differential susceptibility to the effects of parenting. Curr. Opin. Psychol. 15, 125–130 (2017).
Ellis, B. J. & Boyce, W. T. Biological sensitivity to context. Curr. Dir. Psychol. Sci. 17, 183–187 (2008).
Menon, V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 15, 483–506 (2011).
Hendry, A. et al. Developmental change in look durations predicts later effortful control in toddlers at familial risk for ASD. J. Neurodev. Disord. 10, 1–14 (2018).
Hendry, A. et al. Atypical development of attentional control associates with later adaptive functioning, autism and ADHD traits. J. Autism Dev. Disord. 50, 4085–4105 (2020).
Gliga, T. et al. Enhanced visual search in infancy predicts emerging autism symptoms. Curr. Biol. 25, 1727–1730 (2015).
Briggs-Gowan, M. J. & Carter, A. S. Applying the Infant-Toddler Social & Emotional Assessment (ITSEA) and Brief-ITSEA in early intervention. Infant Ment. Health J. 28, 564–583 (2007).
Werchan, D. M., Brandes‐Aitken, A. & Brito, N. H. Signal in the noise: dimensions of predictability in the home auditory environment are associated with neurobehavioral measures of early infant sustained attention. Dev. Psychobiol. 64, e22325 (2022).
Werchan, D. M. & Amso, D. Top-down knowledge rapidly acquired through abstract rule learning biases subsequent visual attention in 9-month-old infants. Dev. Cogn. Neurosci. 42, 100761 (2020).
Richards, J. E. & Anderson, D. R. Attentional inertia in children’s extended looking at television. Adv. Child Dev. Behav. 32, 163–212. https://doi.org/10.1016/S0065-2407(04)80007-7 (2004).
Ludwig, R. J., & Welch, M. G. How babies learn: The autonomic socioemotional reflex. Early Human Development 151, 105183. https://doi.org/10.1016/j.earlhumdev.2020.105183 (2020).
Kingsbury, M. A., & Bilbo, S. D. The inflammatory event of birth: How oxytocin signaling may guide the development of the brain and gastrointestinal system. Front Neuroendocrinol., 55, 100794. https://doi.org/10.1016/j.yfrne.2019.100794 (2019).
Carter, C. S., & Kingsbury, M. A. Oxytocin and oxygen: the evolution of a solution to the ‘stress of life.’ Phil. Trans. R. Soc. B 377 https://doi.org/10.1098/rstb.2021.0054 (2022).
Hane, A. A. et al. The Welch Emotional Connection Screen: validation of a brief mother-infant relational health screen. Acta Paediatrica 108, 615–625. https://doi.org/10.1111/apa.14483 (2029).
Funding
This work was funded by NIH R01MH125870 and the NYU COVID Catalyst grant (to N.H.B.), NIH R01MH126468 (to M.E.T.), and by a NARSAD Young Investigator Grant from the Brain and Behavior Foundation (to D.M.W.).
Author information
Authors and Affiliations
Contributions
D.M.W., C.L.H., M.E.T. and N.H.B. conceptualized the study questions. D.M.W. analyzed the data and wrote the manuscript with input from C.L.H., N.H.B. and M.E.T. A.M.H. and M.Z. collected and coded data. D.M.W., C.L.H. and M.E.T. revised the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
The Institutional Review Board at NYU Langone Health approved all study protocols, and informed written consent was obtained electronically prior to testing. Each participant provided informed consent prior to participation.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Werchan, D.M., Hendrix, C.L., Hume, A.M. et al. Effects of prenatal psychosocial stress and COVID-19 infection on infant attention and socioemotional development. Pediatr Res 95, 1279–1287 (2024). https://doi.org/10.1038/s41390-023-02807-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41390-023-02807-8
This article is cited by
-
Advocate to vaccinate: moving away from the “politics” of vaccination
Pediatric Research (2024)