Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-18T20:25:15.284Z Has data issue: false hasContentIssue false

Stress reactivity in war-exposed young children with and without posttraumatic stress disorder: Relations to maternal stress hormones, parenting, and child emotionality and regulation

Published online by Cambridge University Press:  08 November 2013

Ruth Feldman*
Affiliation:
Bar-Ilan University
Adva Vengrober
Affiliation:
Bar-Ilan University
Moranne Eidelman-Rothman
Affiliation:
Bar-Ilan University
Orna Zagoory-Sharon
Affiliation:
Bar-Ilan University
*
Address correspondence and reprint requests to: Ruth Feldman, Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat Gan, Israel52900; E-mail: Feldman@mail.biu.ac.il.

Abstract

The current study examined biomarkers of stress in war-exposed young children and addressed maternal and child factors that may correlate with children's stress response. Participants were 232 Israeli children aged 1.5–5 years, including 148 children exposed to continuous war. Similarly, 56 were diagnosed with posttraumatic stress disorder (PTSD) and 92 were defined as exposed-no-PTSD. Child cortisol (CT) and salivary alpha amylase (sAA), biomarkers of the hypothalamic–pituitary–adrenal and sympathetic–adrenal–medullary arms of the stress response, were measured at baseline, following challenge, and at recovery. Maternal CT and sAA, PTSD symptoms, and reciprocal parenting, and child negative emotionality and regulatory strategies were assessed. Differences between war-exposed children and controls emerged, but these were related to child PTSD status. Children with PTSD exhibited consistently low CT and sAA, exposed-no-PTSD displayed consistently high CT and sAA, and controls showed increase in CT following challenge and decrease at recovery and low sAA. Exposed children showed higher negative emotionality; however, whereas exposed-no-PTSD children employed comfort-seeking strategies, children with PTSD used withdrawal. Predictors of child CT included maternal CT, PTSD symptoms, low reciprocity, and negative emotionality. Findings suggest that high physiological arousal combined with approach strategies may be associated with greater resilience in the context of early trauma.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allwood, M. A., Bell-Dolan, D., & Husain, S. A. (2002). Children's trauma and adjustment reactions to violent and nonviolent war experiences. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 450457.Google Scholar
Badanes, L. S., Watamura, S. E., & Hankin, B. L. (2011). Hypocortisolism as a potential marker of allostatic load in children: Associations with family risk and internalizing disorders. Development and Psychopathology, 23, 881896.Google Scholar
Bauer, A. M., Quas, J. A., & Boyce, W. T. (2002). Associations between physiological reactivity and children's behavior: Advantages of a multisystem approach. Journal of Developmental and Behavioral Pediatrics, 23, 102113.Google Scholar
Belsky, J. (2008). War, trauma and children's development: Observations from a modern evolutionary perspective. International Journal of Behavioral Development, 32, 260271.CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908.CrossRefGoogle ScholarPubMed
Bosch, J. A., Veerman, E. C. I., de Geus, E. J., & Proctor, G. B. (2011). Alpha amylase as a reliable and convenient measure of sympathetic activity: Don't start salivating just yet! Psychoneuroendocrinology, 36, 449453.CrossRefGoogle ScholarPubMed
Bowlby, J. (1969). Attachment and loss: Vol. 1. Attachment. New York: Basic Books.Google Scholar
Bryce, J. W., Walker, N., Ghorayeb, F., & Kanj, M. (1989). Life experiences, response styles and mental health among mothers and children in Beirut, Lebanon. Social Science Medicine, 28, 685695.Google Scholar
Buss, K. A., Davidson, R. J., Kalin, N. H., & Goldsmith, H. H. (2004). Context-specific freezing and associated physiological reactivity as a dysregulated fear response. Developmental Psychology, 40, 583594.CrossRefGoogle ScholarPubMed
Carrion, V. G., Weems, C. F., Ray, R. D., Glaser, B., Hessl, D., & Reiss, A. L. (2002). Diurnal salivary cortisol in pediatric posttraumatic stress disorder. Biological Psychiatry, 51, 575582.CrossRefGoogle ScholarPubMed
Chemtob, C. M., Nomura, Y., & Abramovitz, R. A. (2008). Impact of conjoined exposure to the World Trade Center attacks and to other traumatic events on the behavioral problems of preschool children. Archives in Pediatric Adolescent Medicine, 162, 126133.CrossRefGoogle Scholar
Chu, A. T., & Lieberman, A. F. (2010). Clinical implications of traumatic stress from birth to age five. Annual Review of Clinical Psychology, 6, 469494.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2001). The impact of child maltreatment and psychopathology on neuroendocrine functioning. Development and Psychopathology, 13, 783804.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2009). Adaptive coping under conditions of extreme stress: Multilevel influences on the determinants of resilience in maltreated children. New Directions for Child and Adolescent Development, 124, 4759.CrossRefGoogle Scholar
Cicchetti, D., & Toth, S. L. (1995). A developmental psychopathology perspective on child abuse and neglect. Journal of the American Academy of Child & Adolescent Psychiatry, 34, 541565.CrossRefGoogle ScholarPubMed
De Bellis, M. D., Baum, A. S., Birmaher, B., Keshavan, M. S., Eccard, C. H., Boring, A. M., et al. (1999). A.E. Bennett Research Award. Developmental traumatology: Part I. Biological stress systems. Biological Psychiatry, 45, 12591270.Google Scholar
Decety, J. (2010). The neurodevelopment of empathy in humans. Developmental Neuroscience, 32, 257267.Google Scholar
Degnan, K. A., Almas, A. N., & Fox, N. A. (2010). Temperament and the environment in the etiology of childhood anxiety. Journal of Child Psychology and Psychiatry, 51, 497517.Google Scholar
Del Giudice, M., Elllis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivitiy. Neuroscience and Biobehavioral Review, 35, 15621592.CrossRefGoogle Scholar
El-Sheikh, M., Erath, S. A., Buckhalt, J. A., Granger, D. A., & Mize, J. (2008). Cortisol and children's adjustment: The moderating role of sympathetic nervous system activity. Journal of Abnormal Child Psychology, 36, 601611.CrossRefGoogle ScholarPubMed
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: Effects on cortisol and behavior. Biological Psychiatry, 52, 776784.CrossRefGoogle ScholarPubMed
Feldman, R. (2007). Parent–infant synchrony and the construction of shared timing: Physiological precursors, developmental outcomes, and risk conditions. Journal of Child Psychology and Psychiatry, 48, 329354.Google Scholar
Feldman, R., & Eidelman, A. I. (2009). Biological and environmental initial conditions shape the trajectories of cognitive and social–emotional development across the first years of life. Developmental Science, 12, 194200.Google Scholar
Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., & Gilboa-Schechtman, E. (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 919927.Google Scholar
Feldman, R., Keren, M., Gross-Rozval, O., & Tyano, S. (2004). Mother–child touch patterns in infant feeding disorders: Relation to maternal, child, and environmental factors. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 10891097.CrossRefGoogle ScholarPubMed
Feldman, R., & Masalha, S. (2010). Parent–child and triadic antecedents of children's social competence: Cultural specificity, shared process. Developmental Psychology, 46, 455467.Google Scholar
Feldman, R., Singer, M., & Zagoory, O. (2010). Touch attenuates infants’ physiological reactivity to stress. Developmental Science, 13, 271278.CrossRefGoogle ScholarPubMed
Feldman, R., & Vengrober, A. (2011). Post-traumatic stress disorder in infants and young children exposed to war-related trauma. Journal of the American Academy of Child & Adolescent Psychiatry, 50, 645658.CrossRefGoogle ScholarPubMed
Feldman, R., Vengrober, A., & Hallaq, E. (2007). Mother–child relationship, child symptoms, and maternal well-being in Israeli and Palestinian infants and young children exposed to war, terror, and violence. Paper presented at the 13th meeting of the European Society for Child and Adolescent Psychiatry, Florence, Italy.Google Scholar
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., et al. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14, 245258.CrossRefGoogle ScholarPubMed
Foa, E. B. (1995). Posttraumatic Stress Diagnostic Scale manual. North Brunswick, NJ: National Computer Systems.Google Scholar
Fombonne, E., Wostear, G., Cooper, V., Harrington, R., & Rutter, M. (2001). The Maudsley long-term follow-up of child and adolescent depression: 2. Suicidality, criminality and social dysfunction in adulthood. British Journal of Psychiatry, 179, 218223.Google Scholar
Fortunato, C. K., Dribin, A. E., Granger, D. A., & Buss, K. A. (2008). Salivary alpha-amylase and cortisol in toddlers: Differential relations to affective behavior. Developmental Psychobiology, 50, 807818. doi: 10.1002/dev.20326Google Scholar
Frigerio, A., Ceppi, E., Rusconi, M., Giorda, R., Raggi, M. E., & Fearon, P. (2009). The role played by the interaction between genetic factors and attachment in the stress response in infancy. Journal of Child Psychology and Psychiatry, 50, 15131522.CrossRefGoogle ScholarPubMed
Fujioka, A., Fujioka, T., Ishida, Y., Maekawa, T., & Nakamura, S. (2006). Differential effects of prenatal stress on the morphological maturation of hippocampal neurons. Neuroscience, 141, 907915.CrossRefGoogle ScholarPubMed
Goldsmith, H., & Rothbart, M. (1996). The Laboratory Temperament Assessment Battery (Lab-TAB): Locomotor version 3.0 technical manual. Madison, WI: University of Wisconsin, Department of Psychology.Google Scholar
Gordis, E. B., Granger, D. A., Susman, E. J., & Trickett, P. K. (2006). Asymmetry between salivary cortisol and alpha-amylase reactivity to stress: Relation to aggressive behavior in adolescents. Psychoneuroendocrinology, 31, 976987.Google Scholar
Gordis, E. B., Margolin, G., Spies, L. A., Susman, E. J., & Granger, D. A. (2010). Interparental aggression and parent–adolescent salivary alpha amylase symmetry. Physiology & Behavior, 100, 225233.CrossRefGoogle ScholarPubMed
Graham, J. E., Christian, L. M., & Kiecolt-Glaser, J. K. (2006), Stress, age, and immune function: Toward a lifespan approach. Journal of Behavioral Medicine, 29, 389400.Google Scholar
Granger, D. A., Kivlighan, K. T., el-Sheikh, M., Gordis, E. B., & Stroud, L. R. (2007). Salivary alpha-amylase in biobehavioral research: Recent developments and applications. Annals of the New York Academy of Sciences, 1098, 122144.Google Scholar
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145173.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Brodersen, L., Nachmias, M., Buss, K., & Rigatuso, J. (1996). Stress reactivity and attachment security. Developmental Psychobiology, 29, 191204.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology, 13, 515538.Google Scholar
Haley, D. W., & Stansbury, K. (2003). Infant stress and parent responsiveness: Regulation of physiology and behavior during still-face and reunion. Child Development, 74, 15341546.Google Scholar
Heim, C., Plotsky, P. M., & Nemeroff, C. B. (2004). Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology, 29, 641648.Google Scholar
Hellhammer, D. H., Wüst, S., & Kudielka, B. M. (2009). Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology, 34, 163171.CrossRefGoogle ScholarPubMed
Hofer, M. A. (1995). Hidden regulators: Implication for a new understanding of attachment, separation, and loss. In Goldberg, S., Muir, R., & Kerr, J. (Eds.), Attachment theory: Social, developmental, and clinical perspectives (pp. 203230). Hillsdale, NJ: Analytic Press.Google Scholar
Juster, R.-P., Bizik, G., Picard, M., Arsenault-Lapierre, G., Sindi, S., Trepanier, L., et al. (2011). A transdisciplinary perspective of chronic stress in relation to psychopathology throughout life span development. Development and Psychopathology, 23, 725776.Google Scholar
King, J. A., Mandansky, D., King, S., Fletcher, K. E., & Brewer, J. (2001). Early sexual abuse and low cortisol. Psychiatry and Clinical Neurosciences, 55, 7174.Google Scholar
Korte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005). The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews, 29, 338.Google Scholar
Laor, N., Wolmer, L., & Cohen, D. J. (2001). Mothers’ functioning and children's symptoms 5 years after a SCUD missile attack. American Journal of Psychiatry, 158, 10201026.CrossRefGoogle ScholarPubMed
Lightman, S. L. (2008). The nueorendocrinology of stress: A never ending story. Journal of Neuroendocrinology, 20, 880884.Google Scholar
Lopes Cardozo, B., Kaiser, R., Gotway, C. A., & Agani, F. (2003). Mental health, social functioning, and feelings of hatred and revenge of Kosovar Albanians one year after the war in Kosovo. Journal of Traumatic Stress, 16, 351360.CrossRefGoogle ScholarPubMed
Masten, A. S., & Narayan, A. J. (2012). Child development in the context of disaster, war, and terrorism: Pathways of risk and resilience. Annual Review of Psychology, 63, 227257.Google Scholar
McEwen, B. S., & Stellar, E. (1993). Stress and the individual: Mechanisms leading to disease. Archives of Internal Medicine, 153, 20932101.Google Scholar
McFarlane, A. C. (2009). Military deployment: The impact on children and family adjustment and the need for care. Current Opinion in Psychiatry, 22, 369373.Google Scholar
Nater, U. M., & Rohleder, N. (2009). Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: Current state of research. Psychoneuroendocrinology, 34, 486496.Google Scholar
Pervanidou, P. (2008). Biology of post-traumatic stress disorder in childhood and adolescence. Journal of Neuroendocrinology, 20, 632638.CrossRefGoogle ScholarPubMed
Pfeffer, C. R., Altemus, M., Heo, M., & Jiang, H. (2007). Salivary cortisol and psychopathology in children bereaved by the September 11, 2001, terror attacks. Biological Psychiatry, 61, 957965.Google Scholar
Pfefferbaum, B., Nixon, S. J., Tucker, P. M., Tivis, R. D., Moore, V. L., Gurwitch, R. H., et al. (1999). Posttraumatic stress responses in bereaved children after the Oklahoma City bombing. Journal of the American Academy of Child & Adolescent Psychiatry, 38, 13721379.Google Scholar
Qouta, S., Punamaki, R. L., & El Sarraj, E. (2003). Prevalence and determinants of PTSD among Palestinian children exposed to military violence. European Child and Adolescence Psychiatry, 12, 265272.CrossRefGoogle ScholarPubMed
Ruttle, P. L., Serbin, L. A., Stack, D. M., Schwartzman, A. E., & Shirtcliff, E. A. (2011). Adrenocortical attunement in mother–child dyads: Importance of situational and behavioral characteristics. Biological Psychology, 88, 104111.CrossRefGoogle ScholarPubMed
Sanson, A., Oberklaid, F., Pedlow, R., & Prior, M. (1991). Risk indicators: Assessment of infancy predictors of pre-school behavioural maladjustment. Journal of Child Psychology and Psychiatry and Allied Disciplines, 32, 609626.Google Scholar
Schaal, S., Jacob, N., Dusingizemungu, J. P., & Elbert, T. (2010). Rates and risks for prolonged grief disorder in a sample of orphaned and widowed genocide survivors. BMC Psychiatry, 10, 55.CrossRefGoogle Scholar
Scheeringa, M. S., Zeanah, C. H., & Cohen, J. A. (2011). PTSD in children and adolescents: Toward an empirically based algorithm. Depression and Anxiety, 28, 770782.Google Scholar
Sethre-Hofstad, L., Stansbury, K., & Rice, M. A. (2002). Attunement of maternal and child adrenocortical response to child challenge. Psychoneuroendocrinology, 27, 731747.CrossRefGoogle ScholarPubMed
Smith, P., Perrin, S., Yule, W., & Rabe-Hesketh, S. (2001). War exposure and maternal reactions in the psychological adjustment of children from Bosnia–Hercegovina. Journal of Child Psychology and Psychiatry, 42, 395404.Google Scholar
Smyth, J. M., Hockemeyer, J. R., & Tulloch, H. (2008). Expressive writing and post-traumatic stress disorder: Effects on trauma symptoms, mood states, and cortisol reactivity. British Journal of Health Psychology, 13, 8593.Google Scholar
Spinrad, T. L., Eisenberg, N., Granger, D. A., Eggum, N. D., Sallquist, J., Haugen, R. G., et al. (2009). Individual differences in preschoolers’ salivary cortisol and alpha-amylase reactivity: Relations to temperament and maladjustment. Hormones and Behavior, 56, 133139.Google Scholar
Spitz, R. (1946). Anaclitic depression. Psychoanalytic Study of the Child, 2, 313342.Google Scholar
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632639.CrossRefGoogle ScholarPubMed
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews, 27, 3344.Google Scholar
Vigil, J. M., Geary, D. C., Granger, D. A., & Flinn, M. V. (2010). Sex differences in salivary cortisol, alpha-amylase, and psychological functioning following Hurricane Katrina. Child Development, 81, 12281240.CrossRefGoogle ScholarPubMed
Wadhwa, P. D. (2005). Psychoneuroendocrine processes in human pregnancy influence fetal development and health. Psychoneuroendocrinology, 30, 724743.CrossRefGoogle ScholarPubMed
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847854.Google Scholar
Weinstock, M. (2005). The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behavior, and Immunology, 19, 296308.Google Scholar
Welberg, L. A., Seckl, J. R., & Holmes, M. C. (2001). Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: Possible implications for behaviour. Neuroscience, 104, 7179.Google Scholar
Wolf, J. M., Nicholls, E., & Chen, E. (2008). Chronic stress, salivary cortisol, and alpha-amylase in children with asthma and healthy children. Biological Psychology, 78, 2028.Google Scholar
Zero to Three. (2005). DC:0–3R: Diagnostic classification of mental health and developmental disorders of infancy and early childhood (rev.). Washington, DC: Author.Google Scholar