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Maternal immune and affiliative biomarkers and sensitive parenting mediate the effects of chronic early trauma on child anxiety

Published online by Cambridge University Press:  11 September 2017

A. Ulmer-Yaniv ,
A. Djalovski ,
K. Yirmiya ,
G. Halevi ,
O. Zagoory-Sharon  and
R. Feldman
A. Ulmer-Yaniv
Affiliation:
The Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel
A. Djalovski
Affiliation:
Department of Psychology, Bar-Ilan University, Ramat-Gan, Israel
K. Yirmiya
Affiliation:
Department of Psychology, Bar-Ilan University, Ramat-Gan, Israel
G. Halevi
Affiliation:
Department of Psychology, Bar-Ilan University, Ramat-Gan, Israel
O. Zagoory-Sharon
Affiliation:
The Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel
R. Feldman*
Affiliation:
The Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel Department of Psychology, Bar-Ilan University, Ramat-Gan, Israel Child Study Center, Yale University, New Haven, Connecticut, USA
*
*Address for correspondence: R. Feldman, Ph.D., Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan 52900, Israel. (Email: feldman.ruth@gmail.com)
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Abstract

Background

Chronic early trauma alters children's stress reactivity and increases the prevalence of anxiety disorders; yet the neuroendocrine and immune mechanisms underpinning this effect are not fully clear. Animal studies indicate that the mother's physiology and behavior mediate offspring stress in a system-specific manner, but few studies tested this external-regulatory maternal role in human children exposed to chronic stress.

Methods

We followed a unique cohort of children exposed to continuous wartime trauma (N = 177; exposed; N = 101, controls; N = 76). At 10 years, maternal and child's salivary immunoglobulin A (s-IgA) and oxytocin (OT), biomarkers of the immune and affiliation systems, were assayed, maternal and child relational behaviors observed, mother and child underwent psychiatric diagnosis, and child anxiety symptoms assessed.

Results

War-exposed mothers had higher s-IgA, lower OT, more anxiety symptoms, and their parenting was characterized by reduced sensitivity. Exposed children showed higher s-IgA, more anxiety disorders and post traumatic stress disorder, and more anxiety symptoms. Path analysis model defined three pathways by which maternal physiology and behavior impacted child anxiety; (a) increasing maternal s-IgA, which led to increased child s-IgA, augmenting child anxiety; (b) reducing maternal OT, which linked with diminished child OT and social repertoire; and (c) increasing maternal anxiety, which directly impacted child anxiety.

Conclusions

Our findings, the first to measure immune and affiliation biomarkers in mothers and children, detail their unique and joint effects on children's anxiety in response to stress; highlight the relations between chronic stress, immune activation, and anxiety in children; and describe how processes of biobehavioral synchrony shape children's long-term adaptation.

Keywords

Childhood anxiety disordersearly life stressmaternal behavioroxytocinsalivary IgAtraumawar exposure
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 6 , April 2018 , pp. 1020 - 1033
Copyright
Copyright © Cambridge University Press 2017 

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References

Achenbach, TM, Rescorla, LA (2000). Manual for the ASEBA preschool forms & profiles: An integrated system of multi-informant assessment; Child behavior checklist for ages 1 1/2-5; Language development survey; Caregiver-teacher report form. University of Vermont.Google Scholar
Bales, KL, Boone, E, Epperson, P, Hoffman, G, Carter, CS (2011). Are behavioral effects of early experience mediated by oxytocin? Frontiers in Psychiatry 2, 24.Google Scholar
Barenbaum, J, Ruchkin, V, Schwab-Stone, M (2004). The psychosocial aspects of children exposed to war: practice and policy initiatives. Journal of Child Psychology and Psychiatry 45, 41–62.Google Scholar
Birmaher, B, Khetarpal, S, Brent, D, Cully, M, Balach, L, Kaufman, J, Neer, SM (1997). The screen for child anxiety related emotional disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry 36, 545–553.Google Scholar
Bosch, JA, Brand, HS, Ligtenberg, AJM, Bermond, B, Hoogstraten, J, Nieuw Amerongen, AV (1998). The response of salivary protein levels and S-IgA to an academic examination are associated with daily stress. Journal of Psychophysiology 12, 384–391.Google Scholar
Bosch, JA, Ring, C, de Geus, EJC, Veerman, ECI, Amerongen, AVN (2002). Stress and secretory immunity. International Review of Neurobiology 52, 213–253.Google Scholar
Carson, DS, Berquist, SW, Trujillo, TH, Garner, JP, Hannah, SL, Hyde, SA, Sumiyoshi, RD, Jackson, LP, Moss, JK, Strehlow, MC, Cheshier, SH, Partap, S, Hardan, AY, Parker, KJ (2014). Cerebrospinal fluid and plasma oxytocin concentrations are positively correlated and negatively predict anxiety in children. Molecular Psychiatry 20, 1–6.Google ScholarPubMed
Chemtob, CM, Nomura, Y, Rajendran, K, Yehuda, R, Schwartz, D, Abramovitz, R (2010). Impact of maternal posttraumatic stress disorder and depression following exposure to the September 11 attacks on preschool children's behavior. Child Development 81, 1129–1141.Google Scholar
Coe, CL, Kramer, M, Kirschbaum, C, Netter, P, Fuchs, E (2002). Prenatal stress diminshes the cytokine response of leukocytes to endotoxin stimulation in juvenile rhesus monkeys. Journal of Clinical Endocrinology and Metabolism 87, 675–681.Google Scholar
Copeland, WE, Shanahan, L, Worthman, C, Angold, A, Costello, EJ (2012). Generalized anxiety and C-reactive protein levels: a prospective, longitudinal analysis. Psychological Medicine 42, 2641–2650.CrossRefGoogle Scholar
Coplan, J, Andrews, M, Rosenblum, L, Owens, M, Friedman, S, Gorman, J, Nemeroff, C (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences of the USA 93, 1619–1623.Google Scholar
Danese, A, McEwen, BS (2012). Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiology & Behavior 106, 29–39.Google Scholar
De Almeida, PDV, Grégio, AMT, Machado, MÂN, De Lima, AAS, Azevedo, LR (2008). Saliva composition and functions: a comprehensive review. Journal of Contemporary Dental Practice 9, 72–80.Google Scholar
Deinzer, R, Kleineidam, C, Stiller-winkler, R, Idel, H, Bachg, D (2000). Prolonged reduction of salivary immunoglobulin A (sIgA) after a major academic exam. International Journal of Psychophysiology 37, 219–232.CrossRefGoogle Scholar
Deinzer, R, Schüller, N (1998). Dynamics of stress-related decrease of salivary immunoglobulin A (sIgA): relationship to symptoms of the common cold and studying behavior. Behavioral Medicine 23, 161–169.Google Scholar
Delongis, A, Coyne, JC, Dakof, G, Folkman, S, Lazarus, RS (1982). Relationship of daily hassles, uplifts, and major life events to health status. Health Psychology 1, 119–136.Google Scholar
DuBois, DL, Felner, RD, Brand, S, Adan, AM, Evans, EG (1992). A prospective study of life stress, social support, and adaptation in early adolescence. Child Development 63, 542–557.Google Scholar
Eckstein, M, Scheele, D, Weber, K, Stoffel-Wagner, B, Maier, W, Hurlemann, R (2014). Oxytocin facilitates the sensation of social stress. Human Brain Mapping 35, 4741–4750.Google Scholar
Engeland, CG, Hugo, FN, Hilgert, JB, Nascimento, GG, Junges, R, Lim, HJ, Marucha, PT, Bosch, JA (2016). Psychological distress and salivary secretory immunity. Brain, Behavior, and Immunity 52, 11–17.Google Scholar
Engert, V, Koester, AM, Riepenhausen, A, Singer, T (2016). Boosting recovery rather than buffering reactivity: higher stress-induced oxytocin secretion is associated with increased cortisol reactivity and faster vagal recovery after acute psychosocial stress. Psychoneuroendocrinology 74, 111–120.CrossRefGoogle ScholarPubMed
Fagundes, CP, Glaser, R, Kiecolt-Glaser, JK (2013). Stressful early life experiences and immune dysregulation across the lifespan. Brain, Behavior, and Immunity 27, 8–12.CrossRefGoogle ScholarPubMed
Feldman, R (1998). Mother-Newborn Coding System Manual. Bar-Ilan University: Bar-Ilan, Israel.Google Scholar
Feldman, R (2010). The relational basis of adolescent adjustment: trajectories of mother–child interactive behaviors from infancy to adolescence shape adolescents’ adaptation. Attachment & Human Development 12, 173–192.CrossRefGoogle ScholarPubMed
Feldman, R (2012a). Oxytocin and social affiliation in humans. Hormones and Behavior 61, 380–391.Google Scholar
Feldman, R (2012b). Parenting behavior as the environment where children grow. In: The Cambridge Handbook of Environment in Human Development (ed. Mayes, L. C., Lewis, M.), pp. 535–568. Cambridge University Press: New York, NY. doi: http://dx.doi.org/10.1017/CBO9781139016827.031.Google Scholar
Feldman, R (2015a). Mutual influences between child emotion regulation and parent–child reciprocity support development across the first 10 years of life: implications for developmental psychopathology. Development and Psychopathology 27, 1007–1023.Google Scholar
Feldman, R (2015b). Sensitive periods in human social development: new insights from research on oxytocin, synchrony, and high-risk parenting. Development and Psychopathology 27, 369–395.Google Scholar
Feldman, R (2016). The neurobiology of mammalian parenting and the biosocial context of human caregiving. Hormones and Behavior 77, 3–17.CrossRefGoogle ScholarPubMed
Feldman, R (2017). The neurobiology of human attachments. Trends in Cognitive Sciences 21, 80–99.Google Scholar
Feldman, R, Bamberger, E, Kanat-Maymon, Y (2013a). Parent-specific reciprocity from infancy to adolescence shapes children's social competence and dialogical skills. Attachment & Human Development 15, 407–423.Google Scholar
Feldman, R, Gordon, I, Influs, M, Gutbir, T, Ebstein, RP (2013b). Parental oxytocin and early caregiving jointly shape children's oxytocin response and social reciprocity. Neuropsychopharmacology 38, 1154–1162.Google Scholar
Feldman, R, Gordon, I, Zagoory-Sharon, O (2010). The cross-generation transmission of Oxytocin in humans. Hormones and Behavior 58, 696–676.Google Scholar
Feldman, R, Gordon, I, Zagoory-Sharon, O (2011). Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. Developmental Science 14, 752–761.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 and Adolescent Psychiatry 48, 919–927.Google Scholar
Feldman, R, Rosenthal, Z, Eidelman, AI (2014a). Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biological Psychiatry 75, 56–64.Google Scholar
Feldman, R, Vengrober, A (2011). Posttraumatic stress disorder in infants and young children exposed to war-related trauma. Journal of the American Academy of Child & Adolescent Psychiatry 50, 645–658.CrossRefGoogle ScholarPubMed
Feldman, R, Vengrober, A, Ebstein, RP (2014b). Affiliation buffers stress: cumulative genetic risk in oxytocin-vasopressin genes combines with early caregiving to predict PTSD in war-exposed young children. Translational Psychiatry 4, e370.Google Scholar
Feldman, R, Vengrober, A, Eidelman-Rothman, M, Zagoory-Sharon, O (2013c). Stress reactivity in war-exposed young children with and without posttraumatic stress disorder: relations to maternal stress hormones, parenting, and child emotionality and regulation. Development and Psychopathology 25, 943–955.CrossRefGoogle ScholarPubMed
Francis, DD, Young, LJ, Meaney, MJ, Insel, TR (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. Journal of Neuroendocrinology 14, 349–353.Google Scholar
Fujimaru, C, Okamura, H, Kawasaki, M, Kakuma, T, Yoshii, C, Matsuishi, T (2012). Self-perceived work-related stress and its relation to salivary IgA, cortisol and 3-methoxy-4-hydroxyphenyl glycol levels among neonatal intensive care nurses. Stress and Health 28, 171–174.Google Scholar
Gallagher, S, Phillips, AC, Evans, P, Der, G, Hunt, K, Carroll, D (2008). Caregiving is associated with low secretion rates of immunoglobulin A in saliva. Brain Behavior, and Immunity 22, 565–572.Google Scholar
Gibney, SM, McGuinness, B, Prendergast, C, Harkin, A, Connor, TJ (2013). Poly I: C-induced activation of the immune response is accompanied by depression and anxiety-like behaviours, kynurenine pathway activation and reduced BDNF expression. Brain, Behavior, and Immunity 28, 170–181.CrossRefGoogle ScholarPubMed
Giovanoli, S, Engler, H, Engler, A, Richetto, J, Voget, M, Willi, R, Winter, C, Riva, MA, Mortensen, PB, Feldon, J, Schedlowski, M, Meyer, U (2013). Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 339, 1095–1099.Google Scholar
Glaser, R, Kiecolt-Glaser, JK (2005). Stress-induced immune dysfunction: implications for health. Nature Reviews Immunology 5, 243–251.Google Scholar
Goodman, R, Ford, T, Richards, H, Gatward, R, Meltzer, H (2000). The Development and Well-Being Assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry 41, 645–655.CrossRefGoogle ScholarPubMed
Grindstaff, JL, Brodie, ED, Ketterson, ED (2003). Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proceedings Biological Sciences/The Royal Society 270, 2309–2319.Google Scholar
Gunnar, M, Quevedo, K (2007). The neurobiology of stress and development. Annual Review of Psychology 58, 145–173.Google Scholar
Hale, WW, Crocetti, E, Raaijmakers, QAW, Meeus, WHJ (2011). A meta-analysis of the cross-cultural psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED). Journal of Child Psychology and Psychiatry and Allied Disciplines 52, 80–90.Google Scholar
Halevi, G, Djalovski, A, Vengrober, A, Feldman, R (2016). Risk and resilience trajectories in war-exposed children across the first decade of life. Journal of Child Psychology and Psychiatry and Allied Disciplines 57, 1183–1193.Google Scholar
Hayes, AF (2013). Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach. Guilford Press.Google Scholar
Heinrichs, M, Baumgartner, T, Kirschbaum, C, Ehlert, U (2003). Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological Psychiatry 54, 1389–1398.Google Scholar
Henningsen, GM, Hurrell, JJ, Baker, F, Douglas, C, MacKenzie, BA, Robertson, SK, Phipps, FC (1992). Measurement of salivary immunoglobulin A as an immunologic biomarker of job stress. Scandinavian Journal of Work, Environment and Health 18(Suppl 2), 133–136.Google Scholar
Herbert, TB, Cohen, S (1993). Stress and immunity in humans: a meta-analytic review. Psychosomatic Medicine 55, 364–379.Google Scholar
Hofer, MA (1994). Hidden regulators in attachment, separation, and loss. Monographs of the Society for Research in Child Development 59, 192–207.Google Scholar
Hofer, MA, Shair, HN (1987). Isolation distress in two-week-old rats: influence of home cage, social companions, and prior experience with littermates. Developmental Psychobiology 20, 465–476.Google Scholar
Hoge, EA, Brandstetter, K, Moshier, S, Pollack, MH, Wong, KK, Simon, NM (2009). Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depression and Anxiety 26, 447–455.Google Scholar
Hoge, EA, Pollack, MH, Kaufman, RE, Zak, PJ, Simon, NM (2008). Oxytocin levels in social anxiety disorder. CNS Neuroscience and Therapeutics 14, 165–170.Google Scholar
Holt-Lunstad, J, Birmingham, W, Light, KC (2011). The influence of depressive symptomatology and perceived stress on plasma and salivary oxytocin before, during and after a support enhancement intervention. Psychoneuroendocrinology 36, 1249–1256.Google Scholar
Hu, L, Bentler, PM (1999). Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal 6, 1–55.Google Scholar
Humphrey, SP, Williamson, RT (2001). A review of saliva: normal composition, flow, and function. The Journal of Prosthetic Dentistry 85, 162–169.Google Scholar
Jensen, SE (2016). Psychological stress and infectious illnesses: one step closer to understanding the mechanisms. Brain, Behavior, and Immunity 52, 9–10.Google Scholar
Joshi, PT, O'Donnell, DA (2003). Consequences of child exposure to war and terrorism. Clinical Child and Family Psychology Review 6, 275–292.Google Scholar
Kay, G, Tarcic, N, Poltyrev, T, Weinstock, M (1998). Prenatal stress depresses immune function in rats. Physiology and Behavior 63, 397–402.Google Scholar
Kendler, KS, Myers, J, Prescott, CA (2017). Parenting and adult mood, anxiety and substance use disorders in female twins: an epidemiological, multi-informant, retrospective study. Psychological Medicine 30, 281–294.Google Scholar
Kirsch, P, Esslinger, C, Chen, Q, Mier, D, Lis, S, Siddhanti, S, Gruppe, H, Mattay, VS, Gallhofer, B, Meyer-Lindenberg, A (2005). Oxytocin modulates neural circuitry for social cognition and fear in humans. Journal of Neuroscience 25, 11489–11493.Google Scholar
Knafo, A, Plomin, R (2006). Prosocial behavior from early to middle childhood: genetic and environmental influences on stability and change. Developmental Psychology 42, 771–786.Google Scholar
Kugler, J, Reintjes, F, Tewes, V, Schedlowski, M (1996). Competition stress in soccer coaches increases salivary. Immunoglobin A and salivary cortisol concentrations. Journal of Sports Medicine and Physical Fitness 36, 117–120.Google Scholar
Kvietkauskaite, R, Vaicaitiene, R, Girkontaite, I, Labeikyte, D (2014). The response of mucosal immunity to stress faced by Lithuanian soldiers as a consequence of deployment to Afghanistan. Balkan Military Medical Review 17, 1.Google Scholar
Labuschagne, I, Phan, KL, Wood, A, Angstadt, M, Chua, P, Heinrichs, M, Stout, JC, Nathan, PJ (2010). Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 35, 2403–2413.Google Scholar
Lasselin, J, Elsenbruch, S, Lekander, M, Axelsson, J, Karshikoff, B, Grigoleit, JS, Engler, H, Schedlowski, M, Benson, S (2016). Mood disturbance during experimental endotoxemia: predictors of state anxiety as a psychological component of sickness behavior. Brain, Behavior, and Immunity 57, 30–37.Google Scholar
Lebowitz, ER, Leckman, JF, Feldman, R, Zagoory-Sharon, O, McDonald, N, Silverman, WK (2016). Salivary oxytocin in clinically anxious youth: associations with separation anxiety and family accommodation. Psychoneuroendocrinology 65, 35–43.Google Scholar
Lee, PR, Brady, DL, Shapiro, RA, Dorsa, DM, Koenig, JI (2007). Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Research 1156, 152–167.Google Scholar
Liu, D, Diorio, J, Tannenbaum, B, Caldji, C, Francis, D, Freedman, A, Sharma, S, Pearson, D, Plotsky, PM, Meaney, MJ (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science (New York, N.Y.) 277, 1659–1662.Google Scholar
Liukkonen, T, Räsänen, P, Jokelainen, J, Leinonen, M, Järvelin, MR, Meyer-Rochow, VB, Timonen, M (2011). The association between anxiety and C-reactive protein (CRP) levels: results from the Northern Finland 1966 birth cohort study. European Psychiatry 26, 363–369.Google Scholar
Lucchina, L, Carola, V, Pitossi, F, Depino, AM (2010). Evaluating the interaction between early postnatal inflammation and maternal care in the programming of adult anxiety and depression-related behaviors. Behavioural Brain Research 213, 56–65.Google Scholar
Luecken, LJ, Lemery, KS (2004). Early caregiving and physiological stress responses. Clinical Psychology Review 24, 171–191.Google Scholar
Lupien, SJ, McEwen, BS, Gunnar, MR, Heim, C (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 10, 434–445.Google Scholar
MacKinnon, DP, Lockwood, CM, Williams, J (2004). Confidence limits for the indirect effect: distribution of the product and resampling methods. Multivariate Behavioral Research 39, 99–128.Google Scholar
Maier, SF, Watkins, LR, Fleshner, M (1994). Psychoneuroimmunology: the interface between behavior, brain, and immunity. American Psychologist 49, 1004–1017.Google Scholar
Mansbach-Kleinfeld, I, Apter, A, Farbstein, I, Levine, SZ, Poznizovsky, A (2010). A population-based psychometric validation study of the Strengths and Difficulties Questionnaire–Hebrew version. Frontiers in Psychiatry 1, 151.Google Scholar
McEwen, BS (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 87, 873–904.Google Scholar
Meyer, U, Feldon, J, Dammann, O (2011). Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatric Research 69(5 Pt 2), 26R–33R. doi: 10.1203/PDR.0b013e318212c196.Google Scholar
Miller, GE, Cohen, S (2001). Psychological interventions and the immune system: a meta-analytic review and critique. Health Psychology: Official Journal of the Division of Health Psychology, American Psychological Association 20, 47–63.Google Scholar
Mousseau, T, Fox, C (1998). The adaptive significance of maternal effects. Trends in Ecology & Evolution 13, 403–407.CrossRefGoogle ScholarPubMed
Musaelyan, K, Egeland, M, Fernandes, C, Pariante, CM, Zunszain, PA, Thuret, S (2014). Modulation of adult hippocampal neurogenesis by early-life environmental challenges triggering immune activation. Neural Plasticity 2014, 194396. doi: 10.1155/2014/194396.Google Scholar
Neumann, ID, Slattery, DA (2016). Oxytocin in general anxiety and social fear: a translational approach. Biological Psychiatry 79, 213–221.Google Scholar
Ng, V, Koh, D, Mok, B, Lim, LP, Yang, Y, Chia, SE (2004). Stressful life events of dental students and salivary immunoglobulin A. International Journal of Immunopathology and Pharmacology 17(2 Suppl), 49–56.Google Scholar
Noonan, LR, Caldwell, JD, Li, L, Walker, CH, Pedersen, CA, Mason, GA (1994). Neonatal stress transiently alters the development of hippocampal oxytocin receptors. Developmental Brain Research 80, 115–120.Google Scholar
Norman, GJ, Hawkley, LC, Cole, SW, Berntson, GG, Cacioppo, JT (2012). Social neuroscience: the social brain, oxytocin, and health. Social Neuroscience 7, 18–29.Google Scholar
O'Connor, TG, Winter, MA, Hunn, J, Carnahan, J, Pressman, EK, Glover, V, Robertson-Blackmore, E, Moynihan, JA, Lee, FE-H, Caserta, MT (2013). Prenatal maternal anxiety predicts reduced adaptive immunity in infants. Brain, Behavior, and Immunity 32, 21–28.Google Scholar
O'Donovan, A, Hughes, BM, Slavich, GM, Lynch, L, Cronin, MT, O'Farrelly, C, Malone, KM (2010). Clinical anxiety, cortisol and interleukin-6: evidence for specificity in emotion-biology relationships. Brain, Behavior, and Immunity 24, 1074–1077.Google Scholar
O'Mahony, SM, Marchesi, JR, Scully, P, Codling, C, Ceolho, AM, Quigley, EMM, Cryan, JF, Dinan, TG (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biological Psychiatry 65, 263–267.Google Scholar
Parker, KJ, Buckmaster, CL, Schatzberg, AF, Lyons, DM (2005). Intranasal oxytocin administration attenuates the ACTH stress response in monkeys. Psychoneuroendocrinology 30, 924–929.Google Scholar
Phillips, AC, Carroll, D, Evans, P, Bosch, JA, Clow, A, Hucklebridge, F, Der, G (2006). Stressful life events are associated with low secretion rates of immunoglobulin A in saliva in the middle aged and elderly. Brain, Behavior, and Immunity 20, 191–197.Google Scholar
Pratt, M, Goldstein, A, Levy, J, Feldman, R (2017). Maternal depression across the first years of life impacts the neural basis of empathy in preadolescence. Journal of the American Academy of Child & Adolescent Psychiatry 56, 20–29.e3.Google Scholar
Pruessner, JC, Kirschbaum, C, Meinlschmid, G, Hellhammer, DH (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28, 916–931.Google Scholar
Quirin, M, Kuhl, J, Düsing Rainer, R (2011). Oxytocin buffers cortisol responses to stress in individuals with impaired emotion regulation abilities. Psychoneuroendocrinology 36, 898–904.Google Scholar
Ramchandani, PG, Domoney, J, Sethna, V, Psychogiou, L, Vlachos, H, Murray, L (2013). Do early father-infant interactions predict the onset of externalising behaviours in young children? Findings from a longitudinal cohort study. Journal of Child Psychology and Psychiatry and Allied Disciplines 54, 56–64.CrossRefGoogle ScholarPubMed
Reichenberg, A, Yirmiya, R, Schuld, A, Kraus, T, Haack, M, Morag, A, Pollmächer, T (2001). Cytokine-associated emotional and cognitive disturbances in humans. Archives of General Psychiatry 58, 445–452.Google Scholar
Rider, MS, Achterberg, J, Lawlis, GF, Goven, A, Toledo, R, Butler, JR (1990). Effect of immune system imagery on secretory IgA. Biofeedback and Self-Regulation 15, 317–333.Google Scholar
Ring, RH, Malberg, JE, Potestio, L, Ping, J, Boikess, S, Luo, B, Schechter, LE, Rizzo, S, Rahman, Z, Rosenzweig-Lipson, S (2006). Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185, 218–225.Google Scholar
Rohrmann, S, Hennig, J, Netter, P (2000). Trait anxiety – possible consequences for health. German Journal of Psychiatry 3, 19–25.Google Scholar
Ross, H, Young, LJ (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Frontiers in Neuroendocrinology 30, 534–547.Google Scholar
Rosseel, Y (2012). Lavaan: an R package for structural equation. Journal of Statistical Software 48, 1–36.Google Scholar
Segerstrom, SC, Miller, GE (2004). Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychological Bulletin 130, 601–630.Google Scholar
Serido, J, Almeida, DM, Wethington, E (2004). Chronic stressors and daily hassles: unique and interactive relationships with psychological distress. Journal of Health and Social Behavior 45, 17–33.Google Scholar
Shamay-Tsoory, SG, Abu-Akel, A (2016). The social salience hypothesis of oxytocin. Biological Psychiatry 79, 194–202.CrossRefGoogle ScholarPubMed
Smith, AS, Wang, Z (2014). Hypothalamic oxytocin mediates social buffering of the stress response. Biological Psychiatry 76, 281–288.Google Scholar
Spielberger, CD, Gorsuch, RL, Lushene, RE (1970). The State-Trait Anxiety Inventory. Consulting Psychologists Press Inc.: Palo Alto, Calif.Google Scholar
Spielberger, CD, Gorsuch, RL, Lushene, PR, Vagg, PR, Jacobs, AG (1983). Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Stone, AA, Cox, DS, Valdimarsdottir, H, Neale, JM (1987). Secretory IgA as a measure of immunocompetence. Journal of Human Stress 13, 136–140.Google Scholar
Sullivan, RM, Holman, PJ (2010). Transitions in sensitive period attachment learning in infancy: the role of corticosterone. Neuroscience & Biobehavioral Reviews 34, 835–844.Google Scholar
Team RC (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.Google Scholar
Team R (2015). RStudio: Integrated Development Environment for R. RStudio, Inc.: Boston, MA.Google Scholar
Tops, M, Van Peer, JM, Korf, J, Wijers, AA, Tucker, DM (2007). Anxiety, cortisol, and attachment predict plasma oxytocin. Psychophysiology 44, 444–449.Google Scholar
Tsujita, S, Morimoto, K (1999). Secretory IgA in saliva can be a useful stress marker. Environmental Health and Preventive Medicine 4, 1–8.Google Scholar
Valdimarsdottir, HB, Stone, AA (1997). Psychosocial factors and secretory immunoglobulin A. Critical Reviews in Oral Biology & Medicine 8, 461–474.Google Scholar
van Ee, E, Kleber, RJ, Mooren, TTM (2012). War trauma lingers on: associations between maternal posttraumatic stress disorder, parent-child interaction, and child development. Infant Mental Health Journal 33, 459–468.Google Scholar
Viena, TD, Banks, JB, Barbu, IM, Schulman, AH, Tartar, JL (2012). Differential effects of mild chronic stress on cortisol and S-IgA responses to an acute stressor. Biological Psychology 91, 307–311.Google Scholar
Vogelzangs, N, Beekman, ATF, de Jonge, P, Penninx, BWJH (2013). Anxiety disorders and inflammation in a large adult cohort. Translational Psychiatry 3, e249.Google Scholar
Walker, AK, Nakamura, T, Byrne, RJ, Naicker, S, Tynan, RJ, Hunter, M, Hodgson, DM (2009). Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology 34, 1515–1525.Google Scholar
Walker, FR, March, J, Hodgson, DM (2004). Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat. Behavioural Brain Research 154, 63–69.Google Scholar
Weaver, ICG, Cervoni, N, Champagne, FA, D'Alessio, AC, Sharma, S, Seckl, JR, Dymov, S, Szyf, M, Meaney, MJ (2004). Epigenetic programming by maternal behavior. Nature Neuroscience 7, 847–854.Google Scholar
Weisman, O, Feldman, R (2013). Oxytocin effects on the human brain: findings, questions, and future directions. Biological Psychiatry 74, 158–159.CrossRefGoogle ScholarPubMed
Weisman, O, Zagoory-Sharon, O, Feldman, R (2013a). Oxytocin administration alters HPA reactivity in the context of parent-infant interaction. European Neuropsychopharmacology 23, 1724–1731.CrossRefGoogle ScholarPubMed
Weisman, O, Zagoory-Sharon, O, Schneiderman, I, Gordon, I, Feldman, R (2013b). Plasma oxytocin distributions in a large cohort of women and men and their gender-specific associations with anxiety. Psychoneuroendocrinology 38, 694–701.Google Scholar
Wohleb, ES, Powell, ND, Godbout, JP, Sheridan, JF (2013). Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. Journal of Neuroscience 33, 13820–13833.Google Scholar
Yang, L, Wang, M, Guo, YY, Sun, T, Li, YJ, Yang, Q, Zhang, K, Liu, SB, Zhao, MG, Wu, YM (2016). Systemic inflammation induces anxiety disorder through CXCL12/CXCR4 pathway. Brain, Behavior, and Immunity 56, 352–362.Google Scholar
Zeier, H, Brauchli, P, Joller-Jemelka, HI (1996). Effects of work demands on immunoglobulin A and cortisol in air traffic controllers. Biological Psychology 42, 413–423.Google Scholar
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