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Stress in pregnancy: Clinical and adaptive behavior of offspring following Superstorm Sandy

Published online by Cambridge University Press:  01 October 2021

Yoko Nomura Open the ORCID record for Yoko Nomura [Opens in a new window] ,
Wei Zhang Open the ORCID record for Wei Zhang [Opens in a new window]  and
Yasmin L. Hurd Open the ORCID record for Yasmin L. Hurd [Opens in a new window]
Yoko Nomura*
Affiliation:
Department of Psychology, CUNY Queens College, Flushing, NY, USA Department of Psychology, CUNY Graduate Center, New York, NY, USA Icahn School of Medicine at Mount Sinai, New York, NY, USA CUNY Graduate School of Public Health & Public Policy, New York, NY, USA
Wei Zhang
Affiliation:
Department of Psychology, New Jersey City University, Jersey City, NJ, USA
Yasmin L. Hurd
Affiliation:
Icahn School of Medicine at Mount Sinai, New York, NY, USA Icahn School of Medicine at Mount Sinai, Neuroscience and Addiction Institute of Mount Sinai, New York, NY, USA
*
Author for Correspondence: Yoko Nomura, CUNY Queens College, Department of Psychology, 65-30 Kissena Blvd, Flushing, NY11367, USA; E-mail: [email protected]
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Abstract

The current study investigated 304 children from a longitudinal project (the Stress in Pregnancy (SIP) Study) who were exposed and unexposed to Superstorm Sandy (“Sandy”) in utero. They were prospectively followed from 2 to 6 years of age and their clinical and adaptive behaviors were assessed annually. Using a hierarchical linear model, the study found that in utero Sandy exposure was associated with greater clinical (anxiety, depression, and somatization) and lower adaptive behaviors (social skills and functional communication) at age 2 years. However, the trajectories were notably different between the two groups. Anxiety increased more rapidly among the exposed than unexposed group at ages 2–4, and depression increased only among the exposed. In contrast, social skills and functional communication were lower in exposed compared to unexposed children at age 2, but quickly increased and exceeded the capacities of unexposed children by age 3. The findings confirm that prenatal Sandy exposure is not only associated with an increase in anxiety, depression, and somatization in offspring, but also with greater adaptive skills as the children got older. Our study demonstrates that while children who have experienced stress in utero demonstrate elevated suboptimal clinical behaviors related to affective disorders, they nevertheless have the potential to learn adaptive skills.

Keywords

clinical and adaptive behaviorsnatural disasterobjective stress exposureprenatal maternal stress
Type
Regular Article
Information
Development and Psychopathology , Volume 34 , Issue 4 , October 2022 , pp. 1249 - 1259
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Barker, D. J. P. (2002). Fetal programming of coronary heart disease. Trends in Endocrinology & Metabolism, 13, 364–368. doi:10.1016/S1043-2760(02)00689-6CrossRefGoogle ScholarPubMed
Bergman, K., Sarkar, P., O'Connor, T. G., Modi, N., Glover, V., & Connor, T. G. O. (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.0b013e31814a62f6CrossRefGoogle ScholarPubMed
Blake, E. S., Kimberlain, T. B., Berg, R. J., Cangialosi, J. P., & Beven, J. L. II (2013). Tropical Cyclone Report Hurricane Sandy Report (AL182012) 22–29 October 2012. Miami, FL: National Hurricane Center.Google Scholar
Bradstreet, L. E., Juechter, J. I., Kamphaus, R. W., Kerns, C. M., & Robins, D. L. (2017). Using the BASC-2 parent rating scales to screen for autism Spectrum disorder in toddlers and preschool-aged children. Journal of Abnormal Child Psychology, 45, 359–370. doi:10.1007/s10802-016-0167-3.CrossRefGoogle ScholarPubMed
Brand, S. R., Engel, S. M., Canfield, R. L., & 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 New York Academy of Sciences, 1071, 454–458. doi:10.1196/annals.1364.041CrossRefGoogle ScholarPubMed
Buitelaar, J. K., Huizink, A. C., Mulder, E. J., de Medina, P. G. R., & Visser, G. H. A. (2003). Prenatal stress and cognitive development and temperament in infants. Neurobiology of Aging, 24, S53–S60. doi:10.1016/S0197-4580(03)00050-2CrossRefGoogle 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.2009.07.010Google ScholarPubMed
Cao, X., Laplante, D. P., Brunet, A., Ciampi, A., & King, S. (2012). Prenatal maternal stress affects motor function in children: Project Ice storm. Developmental Psychobiology, 56, 117–125.CrossRefGoogle ScholarPubMed
CDCP (Centers for Disease Control and Prevention) (2013). Deaths associated with hurricane Sandy — October–November 2012. Morbidity and Mortality Weekly Report, 62, 393–397.Google Scholar
Cohen, J. (1992). Statistical power analysis. Current Directions in Psychological Science, 1, 98–101. doi:10.1111/1467-8721.ep10768783Google Scholar
Davis, E. P., Snidman, N., Wadhwa, P. D., Glynn, L. M., Schetter, C. D., & Sandman, C. A. (2004). Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy, 6, 319–331. doi:10.1207/s15327078in0603_1CrossRefGoogle Scholar
De Brito, S. A., Viding, E., Sebastian, C. L., Kelly, P. A., Mechelli, A., Maris, H., & McCrory, E. J. (2013). Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. Journal of Child Psychology and Psychiatry, 54, 105–112. doi:10.1111/j.1469-7610.2012.02597.x.CrossRefGoogle Scholar
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., & Johnson, T. R. B. (1996). Fetal antecedents of infant temperament. Child Development, 67, 2568–2583. doi:10.1111/j.1467-8624.1996.tb01875.xCrossRefGoogle ScholarPubMed
Dixon, M. L., Thiruchselvam, R., Todd, R., & Christoff, K. (2017). Emotion and the prefrontal cortex: An integrative review. Psychological Bulletin, 143, 1033–1081. doi:10.1037/bul0000096.CrossRefGoogle ScholarPubMed
Edge, M. D., Ramel, W., Drabant, E. M., Kuo, J. R., Parker, K. J., & Gross, J. J. (2009). For better or worse? Stress inoculation effects for implicit but not explicit anxiety. Depression & Anxiety, 26, 831–837. doi:10.1002/da.20592CrossRefGoogle Scholar
Evans, G., & Mills, C. (1998). Identifying class structure: A latent class analysis of the criterion-related and construct validity of the Goldthorpe class schema. European Sociological Review, 14, 87–106.CrossRefGoogle Scholar
Faraone, S. V., Perlis, R. H., Doyle, A. E., Smoller, J. W., Goralnick, J. J., Holmgren, M. A., & Sklar, P. (2005). Molecular genetics of attention-deficit/hyperactivity disorder. Biological Psychiatry, 57, 1313–1323. doi:10.1016/j.biopsych.2004.11.024.CrossRefGoogle ScholarPubMed
Finik, J., & Nomura, Y. (2017). Cohort profile: Stress in Pregnancy (SIP) study. International Journal of Epidemiology, 46, 1388–1388k. doi:10.1093/ije/dyw264Google ScholarPubMed
Fujioka, T., Fujioka, A., Tan, N., Chowdhury, G. M., Mouri, H., Sakata, Y., & Nakamura, S. (2001). Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience, 103, 301–307. doi:10.1016/s0306-4522(00)00582-0CrossRefGoogle ScholarPubMed
Gartstein, M. A., Putnam, S. P., & Rothbart, M. K. (2012). Etiology of preschool behavior problems: Contributions of temperament attributes in early childhood. Infant Mental Health Journal, 33, 197–211.CrossRefGoogle ScholarPubMed
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., … Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala–prefrontal circuitry. Journal of Neurosciences, 33, 4584–4593. doi:10.1523/JNEUROSCI.3446-12.2013Google ScholarPubMed
Glover, V. (2011). Annual research review: Prenatal stress and the origins of psychopathology: An evolutionary perspective. Journal of Child Psychology, Psychiatry and Allied Disciplines, 52, 356–367. doi:10.1111/j.1469-7610.2011.02371.xCrossRefGoogle Scholar
Gold, A. L., Sheridan, M. A., Peverill, M., Busso, D. S., Lambert, H. K., Alves, S., … McLaughlin, K. A. (2016). Childhood abuse and reduced cortical thickness in brain regions involved in emotional processing. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 57, 1154–1164. doi:10.1111/jcpp.12630CrossRefGoogle ScholarPubMed
Hamada, H., & Matthews, S. G. (2019). Prenatal programming of stress responsiveness and behaviours: Progress and perspectives. Journal of Neuroendocrinology, 31, e12674. doi:10.1111/jne.12674.CrossRefGoogle Scholar
Hofstra, M. B., Van Der Ende, J., & Verhulst, F. C. (2002). Child and adolescent problems predict DSM-IV disorders in adulthood: A 14-year follow-up of a Dutch epidemiological sample. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 182–189. doi:10.1097/00004583-200202000-00012CrossRefGoogle ScholarPubMed
Huizink, A. C., Dick, D. M., Sihvola, E., Pulkkinen, L., Rose, R. J., & Kaprio, J. (2007). Chernobyl exposure as stressor during pregnancy and behaviour in adolescent offspring. Acta Psychiatrica Scandinavica, 116, 438–446. doi:10.1111/j.1600-0447.2007.01050.xCrossRefGoogle ScholarPubMed
Jafari, Z., Mehla, J., Kolb, B. l., & Mohajerani, M. H. (2017). Prenatal noise stress impairs HPA axis and cognitive performance in mice. Scientific Reports, 7, 10560. doi:10.1038/s41598-017-09799-6CrossRefGoogle ScholarPubMed
Kamphaus, R. W., Vandeventer, M. C., Brueggemann, A., & Barry, M. (2007). Behavior assessment system for children-second edition. In Smith, S. R., & Handler, L. (Eds.), The clinical assessment of children and adolescents: A practitioner's handbook (pp. 311–326). Mahwah, NJ: Lawrence Erlbaum Associates Publishers.Google Scholar
King, S., & Laplante, D. P. (2005). The effects of prenatal maternal stress on children's cognitive development: Project Ice storm. Stress, 8, 35–45. doi:10.1080/10253890500108391CrossRefGoogle ScholarPubMed
Kuvacic, I., Skrablin, S., Hodzic, D., & Milkovic, G. (1996). Possible influence of expatriation on perinatal outcome. Acta Obstetricia et Gynecologica Scandinavica, 75, 367–371. doi:10.3109/00016349609033333CrossRefGoogle ScholarPubMed
Laplante, D. P., Brunet, A., & King, S. (2016). The effects of maternal stress and illness during pregnancy on infant temperament: Project Ice storm. Pediatric Research, 79, 107–113. doi:10.1038/pr.2015.177CrossRefGoogle ScholarPubMed
Laplante, D. P., Brunet, A., Schmitz, N., Ciampi, A., & King, S. (2008). Project Ice storm: Prenatal maternal stress affects cognitive and linguistic functioning in 5½-year-old children. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 1063–1072. doi:10.1097/CHI.0b013e31817eec80CrossRefGoogle ScholarPubMed
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neurosciences, 23, 155–184. doi:10.1146/annurev.neuro.23.1.155CrossRefGoogle Scholar
Lee, B., Kang, U., Chang, H., & Cho, K. H. (2019). The hidden control architecture of complex brain networks. iScience, 13, 154–162. doi:10.1016/j.isci.2019.02.017CrossRefGoogle ScholarPubMed
Levy, I., & Schiller, D. (2021). Neural computations of threat. Trends in Cognitive Sciences, 25, 151–171. doi:10.1016/j.tics.2020.11.007Google ScholarPubMed
Li, J., Wang, Z. N., Chen, Y. P., Dong, Y. P., Shuai, H. L., & Xiao, X. M. (2012). Late gestational maternal serum cortisol is inversely associated with fetal brain growth. Neuroscience & Biobehavioral Reviews, 36, 1085–1092. doi:10.1016/j.neubiorev.2011.12.006CrossRefGoogle ScholarPubMed
Lin, Y., Xu, J., Huang, J., Jia, Y., Zhang, J., Yan, C., & Zhang, J. (2017). Effects of prenatal and postnatal maternal emotional stress on toddlers’ cognitive and temperamental development. Journal of Affective Disorders, 207, 9–17. doi:10.1016/j.jad.2016.09.010.Google ScholarPubMed
Lorah, J. (2018). Effect size measures for multilevel models: Definition, interpretation, and TIMSS example. Large-scale Assessments in Education, 6, 8. doi:10.1186/s40536-018-0061-2CrossRefGoogle Scholar
Lou, H. C., Hansen, D., Nordentoft, M., Pryds, O., Jensen, F., Nim, J., & Hemmingsen, R. (1994). Prenatal stressors of human life affect fetal brain development. Developmental Medicine & Child Neurology, 36, 826–832. doi:10.1111/j.1469-8749.1994.tb08192.x.CrossRefGoogle ScholarPubMed
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neurosciences, 10, 434–445. doi:10.1038/nrn2639CrossRefGoogle ScholarPubMed
Maas, C. J. M., & Hox, J. J. (2004). The influence of violations of assumptions on multilevel parameter estimates and their standard errors. Computational Statistical Data Analysis, 46, 427–440. doi:10.1016/j.csda.2003.08.006CrossRefGoogle Scholar
Meijer, A. (1985). Child psychiatric sequelae of maternal war stress. Acta Psychiatrica Scandinavica, 72, 505–511. doi:10.1111/j.1600-0447.1985.tb02647.xCrossRefGoogle ScholarPubMed
Mesman, J., & Koot, H. M. (2001 Sep). Early preschool predictors of preadolescent internalizing and externalizing DSM-IV diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 1029–1036. doi:10.1097/00004583-200109000-00011.CrossRefGoogle ScholarPubMed
Milgrom, J., Westley, D. T., & McCloud, P. I. (1995). Do infants of depressed mothers cry more than other infants? Journal of Paediatrics and Child Health, 31, 218–221. doi:10.1111/j.1440-1754.1995.tb00789.xCrossRefGoogle ScholarPubMed
Murray, D., & Cox, J. L. (1990). Screening for depression during pregnancy with the Edinburgh Depression Scale (EPDS). Journal of Reproductive and Infant Psychology, 8, 99–107. doi:10.1080/02646839008403615CrossRefGoogle Scholar
Neumann, D., Herbert, S. E., Peterson, E. R., Underwood, L., Morton, S. M. B., & Waldie, K. E. (2019). A longitudinal study of antenatal and perinatal risk factors in early childhood cognition: Evidence from growing up in New Zealand. Early Human Development, 132, 45–51. doi:10.1016/j.earlhumdev.2019.04.001.CrossRefGoogle ScholarPubMed
Nolvi, S., Karlsson, L., Bridgett, D. J., Korja, R., Huizink, A. C., Kataja, E.-L., & Karlsson, H. (2016). Maternal prenatal stress and infant emotional reactivity six months postpartum. Journal of Affective Disorder, 199, 163–170. doi:10.1016/j.jad.2016.04.020CrossRefGoogle ScholarPubMed
Nomura, Y., Davey, K., Pehme, P. M., Finik, J., Glover, V., Zhang, W., … Ham, J. (2019). Influence of in utero exposure to maternal depression and natural disaster-related stress on infant temperament at 6 months: The children of Superstorm Sandy. Infant Mental Health Journal, 40, 204–216. doi:10.1002/imhj.21766Google ScholarPubMed
Papazoglou, A., & Ferrari, V. (2013). Fast object segmentation in unconstrained video. In Proceedings of the IEEE international conference on computer vision (pp. 1777–1784). doi:10.1109/ICCV.2013.223Google Scholar
Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., … Monk, C. (2016). Alterations in amygdala-prefrontal circuits in infants exposed to prenatal maternal depression. Translational Psychiatry, 6, e935. doi:10.1038/tp.2016.146CrossRefGoogle ScholarPubMed
Qiu, A., Rifkin-Graboi, A., Chen, H., Chong, Y. S., Kwek, K., Gluckman, P. D., … Meaney, M. J. (2013). Maternal anxiety and infants’ hippocampal development: Timing matters. Translational Psychiatry, 3, e306–e306. doi:10.1038/tp.2013.79CrossRefGoogle ScholarPubMed
Raudenbush, S. W., & Bryk, A. S. (2002). Hierarchical linear models: Applications and data analysis methods (2nd ed.). Thousand Oaks, CA: Sage.Google Scholar
Reynolds, C. R., & Kamphaus, R. W. (2004). BASC-2: Behavior assessment system for children (2nd ed.). Circle Pines, MN: American Guidance Service.Google Scholar
Rubonis, A. V., & Bickman, L. (1991). Psychological impairment in the wake of disaster: The disaster–psychopathology relationship. Psychological Bulletin, 109, 384–399. doi:10.1037/0033-2909.109.3.384CrossRefGoogle ScholarPubMed
Schafer, J. L., & Graham, J. W. (2002). Missing data: Our view of the state of the art. Psychological Methods, 7, 147–177. doi:10.1037/1082-989X.7.2.147CrossRefGoogle ScholarPubMed
Spielberger, C. D. (1989). State–trait anxiety inventory: A comprehensive bibliography. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Suzuki, M., Kawagoe, T., Nishiguchi, S., Abe, N., Otsuka, Y., Nakai, R., … Sekiyama, K. (2018). Neural correlates of working memory maintenance in advanced aging: Evidence from fMRI. Frontiers in Aging Neuroscience, 10, 358. doi:10.3389/fnagi.2018.00358CrossRefGoogle ScholarPubMed
Talge, N. M., Neal, C., & Glover, V. (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: How and why? Journal of Child Psychology, Psychiatry, and Allied Disciplines, 48, 245–261. doi:10.1111/j.1469-7610.2006.01714.xCrossRefGoogle ScholarPubMed
Tees, M. T., Harville, E. W., Xiong, X., Buekens, P., Pridjian, G., & Elkind-Hirsch, K. (2010). Hurricane Katrina-related maternal stress, maternal mental health, and early infant temperament. Maternal and Child Health Journal, 14, 511–518. doi:10.1007/s10995-009-0486-xCrossRefGoogle ScholarPubMed
Thompson, E., Kline, E., Ellman, L. M., Mittal, V., Reeves, G. M., & Schiffman, J. (2015 Mar). Emotional and behavioral symptomatology reported by help-seeking youth at clinical high-risk for psychosis. Schizophrenia Research, 162, 79–85. doi:10.1016/j.schres.2015.01.023.CrossRefGoogle ScholarPubMed
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., … Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Sciences, 13, 46–61. doi:10.1111/j.1467-7687.2009.00852.xGoogle ScholarPubMed
van den Bergh, B. R. H., 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.1301450CrossRefGoogle ScholarPubMed
van der Wal, M. F., van Eijsden, M., & Bonsel, G. J. (2007). Stress and emotional problems during pregnancy and excessive infant crying. Journal of Developmental & Behavioral Pediatrics, 28, 431–437. doi:10.1097/DBP.0b013e31811ff8f4CrossRefGoogle ScholarPubMed
Volker, M. A., Lopata, C., Smerbeck, A. M., Knoll, V. A., Thomeer, M. L., Toomey, J. A., & Rodgers, J. D. (2010). BASC-2 PRS profiles for students with high-functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40, 188–199. doi:10.1007/s10803-009-0849-6.CrossRefGoogle ScholarPubMed
Wadhwa, P. D., Sandman, C. A., & Garite, T. J. (2001). Chapter 9 The neurobiology of stress in human pregnancy: Implications for prematurity and development of the fetal central nervous system. Progress in Brain Research, 133, 131–142. doi:10.1016/S0079-6123(01)33010-8CrossRefGoogle Scholar
Yehuda, R., Engel, S. M., Brand, S. R., Seckl, J., Marcus, S. M., & Berkowitz, G. S. (2005). Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. Journal of Clinical Endocrinology & Metabolism, 90, 4115–4118. doi:10.1210/jc.2005-0550CrossRefGoogle Scholar
Yong, P. E., Laplante, D. P., Elgbeili, G., Hillerer, K. M., Brunet, A., O'Hara, M. W., & King, S. (2015). Prenatal maternal stress predicts stress reactivity at 2½ years of age: The Iowa flood study. Psychoneuroendocrinology, 56, 62–78. doi:10.1016/j.psyneuen.2015.02.015CrossRefGoogle Scholar
Zhang, W., Rajendran, K., Ham, J., Finik, J., Buthmann, J., Davey, K., … Nomura, Y. (2018). Prenatal exposure to disaster-related traumatic stress and developmental trajectories of temperament in early childhood: Superstorm Sandy pregnancy study. Journal of Affective Disorder, 234, 335–345. doi:10.1016/j.jad.2018.02.06CrossRefGoogle ScholarPubMed
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