Abstract
Behavioral inhibition (BI) is a risk factor for anxiety. However, the estimates of the strength of this association vary widely. In addition, while BI is a strong predictor of social anxiety disorder (SAD), its association with other anxiety disorders is unclear. The current study sought to establish the relationship between BI and anxiety and to quantify this association for a range of anxiety disorders. We searched PsycInfo, PubMed and Embase for articles published before May 18th, 2019 using search terms for BI, anxiety and prospective study design. We selected articles which assessed the prospective relationship between BI in childhood and anxiety. Using random-effects meta-analysis with robust variance estimation, which allowed for the inclusion of multiple follow-ups of the same sample, we established the association between BI and any anxiety. We also explored the association between BI and individual anxiety disorders. Data from 27 studies consisting of 35 follow-ups of 20 unique samples indicated that BI prospectively increases the odds of anxiety (OR = 2.80, 95% CI 2.03 to 3.86, p < 0.001). There was also a positive association between BI and all individual anxiety disorders, with effect sizes ranging from small in the case of specific phobia (OR = 1.49, 95% CI 1.03 to 2.14, p = 0.03) to large in the case of SAD (OR = 5.84, 95% CI 3.38 to 10.09, p < 0.001). BI in early childhood is a strong risk factor for anxiety. Targeting BI may help reduce the number of children who will develop anxiety disorders.
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References
American Psychiatric Association (1980). Diagnostic and statistical manual of mental disorders: DSM-III (3rd ed.). Washington, DC: American Psychiatric Association.
American Psychiatric Association (1987). Diagnostic and statistical manual of mental disorders: DSM-III-R (3rd ed., rev). Washington, DC: American Psychiatric Association.
American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders: DSM-5 (5thed.). Washington, DC: American Psychiatric Association.
Bandelow, B., & Michaelis, S. (2015). Epidemiology of anxiety disorders in the 21st century. Dialogues in Clinical Neuroscience, 17(3), 327–335.
Barker, T. V., Reeb-Sutherland, B., Degnan, K. A., Walker, O. L., Chronis-Tuscano, A., Henderson, H. A., Pine, D. S., & Fox, N. A. (2015). Contextual startle responses moderate the relation between behavioral inhibition and anxiety in middle childhood. Psychophysiology, 52(11), 1544–1549. https://doi.org/10.1111/psyp.12517.
Baxter, A. J., Vos, T., Scott, K. M., Ferrari, A. J., & Whiteford, H. A. (2014). The global burden of anxiety disorders in 2010. Psychological Medicine, 44(11), 2363–2374. https://doi.org/10.1017/S0033291713003243.
Biederman, J., Rosenbaum, J. F., Bolduc-Murphy, E. A., Faraone, S. V., Chaloff, J., Hirshfeld, D. R., & Kagan, J. (1993). A 3-year follow-up of children with and without behavioral inhibition. Journal of the American Academy of Child and Adolescent Psychiatry, 32(4), 814–821. https://doi.org/10.1097/00004583-199307000-00016.
Bohlin, G., & Hagekull, B. (2009). Socio-emotional development: From infancy to young adulthood. Scandinavian Journal of Psychology, 50(6), 592–601. https://doi.org/10.1111/j.1467-9450.2009.00787.x.
Borenstein, M. , Hedges, L. V., Higgins, J. P. & Rothstein, H. R. (2009). Publication Bias. In introduction to meta-analysis (pg 277–297), Publication Bias.
Bourdon, J. L., Savage, J. E., Verhulst, B., Carney, D. M., Brotman, M. A., Pine, D. S., Leibenluft, E., Roberson-Nay, R., & Hettema, J. M. (2019). The genetic and environmental relationship between childhood behavioral inhibition and preadolescent anxiety. Twin Research and Human Genetics : The Official Journal of the International Society for Twin Studies, 22(1), 48–55. https://doi.org/10.1017/thg.2018.73.
Buss, K. A. (2011). Which fearful toddlers should we worry about? Context, fear regulation, and anxiety risk. Developmental Psychology, 47(3), 804–819. https://doi.org/10.1037/a0023227.
Buzzell, G. A., Troller-Renfree, S. V., Barker, T. V., Bowman, L. C., Chronis-Tuscano, A., Henderson, H. A., Kagan, J., Pine, D. S., & Fox, N. A. (2017). A neurobehavioral mechanism linking behaviorally inhibited temperament and later adolescent social anxiety. Journal of the American Academy of Child and Adolescent Psychiatry, 56(12), 1097–1105. https://doi.org/10.1016/j.jaac.2017.10.007.
Caspi, A., Moffitt, T. E., Newman, D. L., & Silva, P. A. (1996). Behavioral observations at age 3 years predict adult psychiatric disorders. Longitudinal evidence from a birth cohort. Archives of General Psychiatry, 53(11), 1033–1039.
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., Raggi, V. L., & Fox, N. A. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 48(9), 928–935. https://doi.org/10.1097/CHI.0b013e3181ae09df.
Chronis-Tuscano, A., Rubin, K. H., O’Brien, K. A., Coplan, R. J., Thomas, S. R., Dougherty, L. R., et al. (2015). Preliminary evaluation of a multimodal early intervention program for behaviorally inhibited preschoolers. Journal of Consulting and Clinical Psychology, 83(3), 534–540. https://doi.org/10.1037/a0039043.
Clauss, J. A., & Blackford, J. U. (2012). Behavioral inhibition and risk for developing social anxiety disorder: A meta-analytic study. Journal of the American Academy of Child and Adolescent Psychiatry, 51(10), 1066–1075.e1. https://doi.org/10.1016/j.jaac.2012.08.002.
Colonnesi, C., Draijer, E. M., Stams, G. J. J. M., der Bruggen, C. O. V., Bögels, S. M., & Noom, M. J. (2011). The relation between insecure attachment and child anxiety: A meta-analytic review. Journal of Clinical Child & Adolescent Psychology, 40(4), 630–645. https://doi.org/10.1080/15374416.2011.581623.
Dyson, M. W., Klein, D. N., Olino, T. M., Dougherty, L. R., & Durbin, C. E. (2011). Social and non-social behavioral inhibition in preschool-age children: Differential associations with parent-reports of temperament and anxiety. Child Psychiatry and Human Development, 42(4), 390–405. https://doi.org/10.1007/s10578-011-0225-6.
Edwards, S. L., Rapee, R. M., & Kennedy, S. (2010). Prediction of anxiety symptoms in preschool-aged children: Examination of maternal and paternal perspectives. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 51(3), 313–321. https://doi.org/10.1111/j.1469-7610.2009.02160.x.
Essex, M. J., Klein, M. H., Slattery, M. J., Goldsmith, H. H., & Kalin, N. H. (2010). Early risk factors and developmental pathways to chronic high inhibition and social anxiety disorder in adolescence. The American Journal of Psychiatry, 167(1), 40–46. https://doi.org/10.1176/appi.ajp.2010.167.5.a40.
Frenkel, T. I., Fox, N. A., Pine, D. S., Walker, O. L., Degnan, K. A., & Chronis-Tuscano, A. (2015). Early childhood behavioral inhibition, adult psychopathology and the buffering effects of adolescent social networks: A twenty-year prospective study. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 56(10), 1065–1073. https://doi.org/10.1111/jcpp.12390.
Grant, V. V., Bagnell, A. L., Chambers, C. T., & Stewart, S. H. (2009). Early temperament prospectively predicts anxiety in later childhood. Canadian Journal of Psychiatry. Revue Canadienne de Psychiatrie, 54(5), 320–330. https://doi.org/10.1177/070674370905400506.
Henderson, H. A., Pine, D. S., & Fox, N. A. (2015). Behavioral inhibition and developmental risk: A dual-processing perspective. Neuropsychopharmacology, 40(1), 207–224. https://doi.org/10.1038/npp.2014.189.
Hirshfeld, D. R., Rosenbaum, J. F., Biederman, J., Bolduc, E. A., Faraone, S. V., Snidman, N., et al. (1992). Stable behavioral inhibition and its association with anxiety disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 31(1), 103–111. https://doi.org/10.1097/00004583-199201000-00016.
Hirshfeld-Becker, D. R., & Biederman, J. (2002). Rationale and principles for early intervention with young children at risk for anxiety disorders. Clinical Child and Family Psychology Review, 5(3), 161–172.
Hirshfeld-Becker, D. R., Biederman, J., Henin, A., Faraone, S. V., Davis, S., Harrington, K., & Rosenbaum, J. F. (2007). Behavioral inhibition in preschool children at risk is a specific predictor of middle childhood social anxiety: A five-year follow-up. Journal of Developmental and Behavioral Pediatrics: JDBP, 28(3), 225–233. https://doi.org/10.1097/01.DBP.0000268559.34463.d0.
Hirshfeld-Becker, D. R., Masek, B., Henin, A., Blakely, L. R., Pollock-Wurman, R. A., McQuade, J., DePetrillo, L., Briesch, J., Ollendick, T. H., Rosenbaum, J. F., & Biederman, J. (2010). Cognitive behavioral therapy for 4- to 7-year-old children with anxiety disorders: A randomized clinical trial. Journal of Consulting and Clinical Psychology, 78(4), 498–510. https://doi.org/10.1037/a0019055.
Howes Vallis, E., Zwicker, A., Uher, R., & Pavlova, B. (2019). Cognitive-behavioral intervention for prevention and treatment of anxiety in preschool children: A systematic review and meta-analysis. Submitted.
Hudson, J. L., & Dodd, H. F. (2012). Informing early intervention: Preschool predictors of anxiety disorders in middle childhood. PLoS One, 7(8), e42359. https://doi.org/10.1371/journal.pone.0042359.
Hudson, J. L., Dodd, H. F., Lyneham, H. J., & Bovopoulous, N. (2011). Temperament and family environment in the development of anxiety disorder: Two-year follow-up. Journal of the American Academy of Child and Adolescent Psychiatry, 50(12), 1255–1264.e1. https://doi.org/10.1016/j.jaac.2011.09.009.
Hudson, J. L., Murayama, K., Meteyard, L., Morris, T., & Dodd, H. F. (2018). Early childhood predictors of anxiety in early adolescence. Journal of Abnormal Child Psychology., 47, 1121–1133. https://doi.org/10.1007/s10802-018-0495-6.
Jackson, D., & Turner, R. (2017). Power analysis for random-effects meta-analysis. Research Synthesis Methods, 8(3), 290–302. https://doi.org/10.1002/jrsm.1240.
Johnson, V. C., Kryski, K. R., Sheikh, H. I., Smith, H. J., Singh, S. M., & Hayden, E. P. (2016). The serotonin transporter promoter polymorphism moderates the continuity of behavioral inhibition in early childhood. Development and Psychopathology, 28(4pt1), 1103–1116. https://doi.org/10.1017/S0954579416000729.
Kagan, J., Snidman, N., Zentner, M., & Peterson, E. (1999). Infant temperament and anxious symptoms in school age children. Development and Psychopathology, 11(2), 209–224.
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62(6), 593–602. https://doi.org/10.1001/archpsyc.62.6.593.
Kim-Cohen, J., Caspi, A., Moffitt, T. E., Harrington, H., Milne, B. J., & Poulton, R. (2003). Prior juvenile diagnoses in adults with mental disorder: Developmental follow-back of a prospective-longitudinal cohort. Archives of General Psychiatry, 60(7), 709–717. https://doi.org/10.1001/archpsyc.60.7.709.
Kingston, D., Heaman, M., Brownell, M., & Ekuma, O. (2015). Predictors of childhood anxiety: A population-based cohort study. PLoS One, 10(7), e0129339. https://doi.org/10.1371/journal.pone.0129339.
Kmet, L., Lee, R., & Cook, L. (2004). Standard quality assessment criteria for evaluating primary research papers from a variety of fields. Edmonton, AL: Alberta Heritage Foundation for Medical Research Edmonton.
Lahat, A., Benson, B. E., Pine, D. S., Fox, N. A., & Ernst, M. (2018). Neural responses to reward in childhood: Relations to early behavioral inhibition and social anxiety. Social Cognitive and Affective Neuroscience, 13(3), 281–289. https://doi.org/10.1093/scan/nsw122.
Lau, E. X., Rapee, R. M., & Coplan, R. J. (2017). Combining child social skills training with a parent early intervention program for inhibited preschool children. Journal of Anxiety Disorders, 51, 32–38. https://doi.org/10.1016/j.janxdis.2017.08.007.
Lewis, A. J., & Olsson, C. A. (2011). Early life stress and child temperament style as predictors of childhood anxiety and depressive symptoms: Findings from the longitudinal study of Australian children [research article]. doi: https://doi.org/10.1155/2011/296026.
Majdandžić, M., de Vente, W., Colonnesi, C., & Bögels, S. M. (2018). Fathers’ challenging parenting behavior predicts less subsequent anxiety symptoms in early childhood. Behaviour Research and Therapy, 109, 18–28. https://doi.org/10.1016/j.brat.2018.07.007.
McLeod, B. D., Wood, J. J., & Weisz, J. R. (2007). Examining the association between parenting and childhood anxiety: A meta-analysis. Clinical Psychology Review, 27(2), 155–172. https://doi.org/10.1016/j.cpr.2006.09.002.
Mian, N. D., Wainwright, L., Briggs-Gowan, M. J., & Carter, A. S. (2011). An ecological risk model for early childhood anxiety: The importance of early child symptoms and temperament. Journal of Abnormal Child Psychology, 39(4), 501–512. https://doi.org/10.1007/s10802-010-9476-0.
Micco, J. A., Henin, A., Mick, E., Kim, S., Hopkins, C. A., Biederman, J., & Hirshfeld-Becker, D. R. (2009). Anxiety and depressive disorders in offspring at high risk for anxiety: A meta-analysis. Journal of Anxiety Disorders, 23(8), 1158–1164. https://doi.org/10.1016/j.janxdis.2009.07.021.
Moffitt, T. E., Caspi, A., Harrington, H., Milne, B. J., Melchior, M., Goldberg, D., & Poulton, R. (2007). Generalized anxiety disorder and depression: Childhood risk factors in a birth cohort followed to age 32. Psychological Medicine, 37(3), 441–452. https://doi.org/10.1017/S0033291706009640.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group, T. P. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Medicine, 6(7), e1000097. https://doi.org/10.1371/journal.pmed.1000097.
Möller, E. L., Nikolić, M., Majdandžić, M., & Bögels, S. M. (2016). Associations between maternal and paternal parenting behaviors, anxiety and its precursors in early childhood: A meta-analysis. Clinical Psychology Review, 45, 17–33. https://doi.org/10.1016/j.cpr.2016.03.002.
Muris, P., van Brakel, A. M. L., Arntz, A., & Schouten, E. (2011). Behavioral inhibition as a risk factor for the development of childhood anxiety disorders: A longitudinal study. Journal of Child and Family Studies, 20(2), 157–170. https://doi.org/10.1007/s10826-010-9365-8.
Nepon, J., Belik, S.-L., Bolton, J., & Sareen, J. (2010). The relationship between anxiety disorders and suicide attempts: Findings from the National Epidemiologic Survey on alcohol and related conditions. Depression and Anxiety, 27(9), 791–798. https://doi.org/10.1002/da.20674.
Park, M.-H., Sanders, E., Howe, M., Singh, M., Hallmayer, J., Kim, E., & Chang, K. (2015). Association of Anxiety Symptoms in offspring of bipolar parents with serotonin transporter-linked polymorphic region (5-HTTLPR) genotype. Journal of Child and Adolescent Psychopharmacology, 25(6), 458–466. https://doi.org/10.1089/cap.2014.0115.
Polanin, J. R., & Snilstveit, B. (2016). Campbell methods policy note on converting between effect sizes. Oslo: The Campbell Collaboration, 1, 1.
Prior, M., Smart, D., Sanson, A., & Oberklaid, F. (2000). Does shy-inhibited temperament in childhood lead to anxiety problems in adolescence? Journal of the American Academy of Child and Adolescent Psychiatry, 39(4), 461–468. https://doi.org/10.1097/00004583-200004000-00015.
Rapee, R. M. (2014). Preschool environment and temperament as predictors of social and nonsocial anxiety disorders in middle adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 53(3), 320–328. https://doi.org/10.1016/j.jaac.2013.11.014.
Rapee, R. M., Schniering, C. A., & Hudson, J. L. (2009). Anxiety disorders during childhood and adolescence: Origins and treatment. Annual Review of Clinical Psychology, 5, 311–341. https://doi.org/10.1146/annurev.clinpsy.032408.153628.
Rubin, K. H., Coplan, R. J., & Bowker, J. C. (2009). Social withdrawal in childhood. Annual Review of Psychology, 60, 141–171. https://doi.org/10.1146/annurev.psych.60.110707.163642.
Ryan, S. M., & Ollendick, T. H. (2018). The interaction between child behavioral inhibition and parenting behaviors: Effects on internalizing and externalizing symptomology. Clinical Child and Family Psychology Review, 21(3), 320–339. https://doi.org/10.1007/s10567-018-0254-9.
Schwartz, C. E., Snidman, N., & Kagan, J. (1999). Adolescent social anxiety as an outcome of inhibited temperament in childhood. Journal of the American Academy of Child and Adolescent Psychiatry, 38(8), 1008–1015. https://doi.org/10.1097/00004583-199908000-00017.
Statacorp. (2017). Stata statistical software: Release 15. College Station, TX: StataCorp LLC.
Stein, M. B., & Stein, D. J. (2008). Social anxiety disorder. Lancet (London, England), 371(9618), 1115–1125. https://doi.org/10.1016/S0140-6736(08)60488-2.
Stumper, A., Danzig, A. P., Dyson, M. W., Olino, T. M., Carlson, G. A., & Klein, D. N. (2017). Parents’ behavioral inhibition moderates association of preschoolers’ BI with risk for age 9 anxiety disorders. Journal of Affective Disorders, 210, 35–42. https://doi.org/10.1016/j.jad.2016.12.008.
Talati, A., Odgerel, Z., Wickramaratne, P. J., Norcini-Pala, A., Skipper, J. L., Gingrich, J. A., & Weissman, M. M. (2017). Associations between serotonin transporter and behavioral traits and diagnoses related to anxiety. Psychiatry Research, 253, 211–219. https://doi.org/10.1016/j.psychres.2017.03.033.
Tanner-Smith, E. E., & Tipton, E. (2014). Robust variance estimation with dependent effect sizes: Practical considerations including a software tutorial in Stata and spss. Research Synthesis Methods, 5(1), 13–30. https://doi.org/10.1002/jrsm.1091.
Volbrecht, M. M., & Goldsmith, H. H. (2010). Early temperamental and family predictors of shyness and anxiety. Developmental Psychology, 46(5), 1192–1205. https://doi.org/10.1037/a0020616.
Vreeke, L. J., Muris, P., Mayer, B., Huijding, J., & Rapee, R. M. (2013). Skittish, shielded, and scared: Relations among behavioral inhibition, overprotective parenting, and anxiety in native and non-native Dutch preschool children. Journal of Anxiety Disorders, 27(7), 703–710. https://doi.org/10.1016/j.janxdis.2013.09.006.
White, L. K., Degnan, K. A., Henderson, H. A., Pérez-Edgar, K., Walker, O. L., Shechner, T., Leibenluft, E., Bar-Haim, Y., Pine, D. S., & Fox, N. A. (2017). Developmental relations between behavioral inhibition, anxiety, and attention biases to threat and positive information. Child Development, 88(1), 141–155. https://doi.org/10.1111/cdev.12696.
Wichstrøm, L., Belsky, J., & Berg-Nielsen, T. S. (2013). Preschool predictors of childhood anxiety disorders: A prospective community study. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 54(12), 1327–1336. https://doi.org/10.1111/jcpp.12116.
Wilson, D.B. (2000). Practical meta-analysis effect size calculator [online calculator]. Campbell Collaboration. Retrieved from https:/www.campbellcollaboration.org/research-resources/research-for-resources/effect-size-calculator.html.
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The authors report no conflicts of interest. The work leading to this publication has been supported by funding from the Canada Research Chairs Programs, Nova Scotia Health Research Foundation, and The Dalhousie Department of Psychiatry Summer Studentship Program.
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Sandstrom, A., Uher, R. & Pavlova, B. Prospective Association between Childhood Behavioral Inhibition and Anxiety: a Meta-Analysis. Res Child Adolesc Psychopathol 48, 57–66 (2020). https://doi.org/10.1007/s10802-019-00588-5
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DOI: https://doi.org/10.1007/s10802-019-00588-5