Stress Response Profiles and Physical Aggression in Early Childhood
DOI:
https://doi.org/10.14738/assrj.118.17506Keywords:
adaptive calibration model, autonomic nervous system, hypothalamic pituitary adrenal axis, latent profile analysis, physical aggressionAbstract
This study examined the applicability of the four stress response patterns proposed by the Adaptive Calibration Model (ACM; Del Giudice et al., 2011) in 12-month-old children (N = 214; 116 boys) and their associations with physical aggression at 12, 20, and 30 months of age. Salivary alpha-amylase (sAA) and pre-ejection period (PEP) served as indices of the sympathetic nervous system, respiratory sinus arrhythmia as an index of the parasympathetic nervous system, salivary cortisol as an index of the hypothalamic-pituitary-adrenal axis, and heart rate as a measure of overall autonomic nervous system activity. A fear challenge was administered at 12 months to measure baseline, response, and recovery levels of the stress systems, while maternal reports were used to evaluate physical aggression at the various time points. Through latent profile analysis, three stress response profiles were identified: (1) ANS Responders, (2) Moderate Responders (across all stress systems), and (3) Hormonal Responders. Despite some deviations, each profile could be associated with a corresponding ACM stress response pattern, primarily due to the inclusion of both sAA and PEP as measures of sympathetic activity. At 12 months, ANS Responders showed higher levels of physical aggression, whereas Hormonal Responders exhibited higher levels of physical aggression at 20 months. The findings confirm that differences in stress response patterns can be observed as early as 12 months of age. Moreover, this study emphasizes the importance of using multiple indices of stress responsivity to identify such distinct patterns. Finally, stress response profiles that differ from the most common (moderate) profile, are associated (albeit not consistently) with higher levels of physical aggression at different ages during early childhood.
References
Alink, L. R. A., Mesman, J., Van Zeijl, J., Stolk, M. N., Juffer, F., Koot, H. M., Bakermans-Kranenburg, M. J., & Van IJzendoorn, M. H. (2006). The early childhood aggression curve: Development of physical aggression in 10- to 50-month-old children. Child Development, 77(4), 954–966. https://doi.org/10.1111/j.1467-8624.2006.00912.x
Alkon, A., Boyce, W. T., Davis, N. V., & Eskenazi, B. (2011). Developmental changes in autonomic nervous system resting and reactivity measures in Latino children from 6 to 60 months of age. Journal of Developmental & Behavioral Pediatrics, 32(9), 668–677. https://doi.org/10.1097/dbp.0b013e3182331fa6
Baker, E. C., Baibazarova, E., Ktistaki, G., Shelton, K. H., & Van Goozen, S. H. M. (2012). Development of fear and guilt in young children: Stability over time and relations with psychopathology. Development and Psychopathology, 24(3), 833–845. https://doi.org/10.1017/S0954579412000399
Baker, E., Shelton, K. H., Baibazarova, E., Hay, D. F., & Van Goozen, S. H. (2013). Low skin conductance activity in infancy predicts aggression in toddlers 2 years later. Psychological Science, 24(6), 1051–1056.
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 & Behavioral Pediatrics, 23(2), 102–113. http://dx.doi.org/10.1097/00004703-200204000-00007
Beauchaine, T. P., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74(2), 174–184. https://doi.org/10.1016/j.biopsycho.2005.08.008
Bornstein, M. H., & Suess, P. E. (2000). Child and mother cardiac vagal tone: continuity, stability, and concordance across the first 5 years. Developmental Psychology, 36(1), 54–65. https://doi.org/10.1037/0012-1649.36.1.54
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17(2), 271–301.
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. The British Journal of Psychiatry, 179(2), 144–150. https://doi.org/10.1192/bjp.179.2.144
Brewer-Smyth, K., Burgess, A. W., & Shults, J. (2004). Physical and sexual abuse, salivary cortisol, and neurologic correlates of violent criminal behavior in female prison inmates. Biological Psychiatry, 55(1), 21–31. https://doi.org/10.1016/S0006-3223(03)00705-4
Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74(2), 144–153. https://doi.org/10.1016/j.biopsycho.2006.09.005
Campbell, S. B., Spieker, S., Burchinal, M., & Poe, M. D. (2006). Trajectories of aggression from toddlerhood to age 9 predict academic and social functioning through age 12. Journal of Child Psychology and Psychiatry and Allied Disciplines, 47(8), 791–800. https://doi.org/10.1111/j.1469-7610.2006.01636.x
Chen, F. R., Raine, A., & Granger, D. A. (2015). Tactics for modeling multiple salivary analyte data in relation to behavior problems: Additive, ratio, and interaction effects. Psychoneuroendocrinology, 51, 188–200.
Clark, S. L., & Muthén, B. (2009). Relating latent class analysis results to variables not included in the analysis. Mplus. http://statmodel.com/download/relatinglca.pdf
Côté, S., Vaillancourt, T., LeBlanc, J. C., Nagin, D. S., & Tremblay, R. E. (2006). The development of physical aggression from toddlerhood to pre-adolescence: A nation wide longitudinal study of Canadian children. Journal of Abnormal Child Psychology, 34(1), 71–85. https://doi.org/10.1007/s10802-005-9001-z
Davis, E. P., & Granger, D. A. (2009). Developmental differences in infant salivary alpha-amylase and cortisol responses to stress. Psychoneuroendocrinology, 34(6), 795–804.
De Geus, E. J. C., Willemsen, G. H. M., Klaver, C. H. A. M., & Van Doornen, L. J. P. (1995). Ambulatory measurement of respiratory sinus arrhythmia and respiration rate. Biological Psychology, 41(3), 205–227. https://doi.org/10.1016/0301-0511(95)05137-6
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The Adaptive Calibration Model of stress responsivity. Neuroscience and Biobehavioral Reviews, 35(7), 1562–1592. https://doi.org/10.1016/j.neubiorev.2010.11.007
Del Giudice, M., Hinnant, J. B., Ellis, B. J., & El-Sheikh, M. (2012). Adaptive patterns of stress responsivity: A preliminary investigation. Developmental Psychology, 48(3), 775–790. https://doi.org/10.1037/a0026519
Dierckx, B., Kok, R., Tulen, J. H., Jaddoe, V. W., Hofman, A., Verhulst, F. C., Bakermans-Kranenburg, M. J., Van IJzendoorn, M. H., & Tiemeier, H. (2014). A prospective study of heart rate and externalising behaviours in young children. Journal of Child Psychology and Psychiatry, 55(4), 402–410. https://doi.org/10.1111/jcpp.12175
Dietrich, A., Riese, H., Sondeijker, F. E., Greaves-Lord, K., Ormel, J., Neeleman, J., & Rosmalen, J. G. (2007). Externalizing and internalizing problems in relation to autonomic function: A population-based study in preadolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 46(3), 378–386. https://doi.org/10.1097/CHI.0b013e31802b91ea
Ellis, B. J., & Boyce, W. T. (2008). Biological sensitivity to context. Current Directions in Psychological Science, 17(3), 183–187. https://doi.org/10.1111/j.1467-8721.2008.00571.x
Ellis, B. J., Oldehinkel, A. J., & Nederhof, E. (2017). The adaptive calibration model of stress responsivity: An empirical test in the Tracking Adolescents’ Individual Lives Survey study. Development and Psychopathology, 29(3), 1001–1021 https://doi.org/10.1017/S0954579416000985
El-Sheikh, M., Harger, J., & Whitson, S. M. (2001). Exposure to interparental conflict and children's adjustment and physical health: The moderating role of vagal tone. Child Development, 72(6), 1617–1636. https://doi.org/10.1111/1467-8624.00369
El-Sheikh, M., Hinnant, J. B., & Erath, S. (2011). Developmental trajectories of delinquency symptoms in childhood: The role of marital conflict and autonomic nervous system activity. Journal of Abnormal Psychology, 120(1), 16–32. https://doi.org/10.1037/a0020626
Engeland, C. G., Bosch, J. A., & Rohleder, N. (2019). Salivary biomarkers in psychoneuroimmunology. Current opinion in behavioral sciences, 28, 58–65. https://doi.org/10.1016/j.cobeha.2019.01.007
Engert, V., Vogel, S., Efanov, S. I., Duchesne, A., Corbo, V., Ali, N., & Pruessner, J. C. (2011). Investigation into the cross-correlation of salivary cortisol and alpha-amylase responses to psychological stress. Psychoneuroendocrinology, 36(9), 1294–1302. https://doi.org/10.1016/j.psyneuen.2011.02.018
Gerra, G., Zaimovic, A., Avanzini, P., Chittolini, B., Giucastro, G., Caccavari, R., ... & Brambilla, F. (1997). Neurotransmitter-neuroendocrine responses to experimentally induced aggression in humans: influence of personality variable. Psychiatry Research, 66(1), 33–43. https://doi.org/10.1016/S0165-1781(96)02965-4
Goldberg, S., Levitan, R., Leung, E., Masellis, M., Basile, V. S., Nemeroff, C. B., & Atkinson, L. (2003). Cortisol concentrations in 12-to 18-month-old infants: Stability over time, location, and stressor. Biological Psychiatry, 54(7), 719–726. https://doi-org.vu-nl.idm.oclc.org/10.1016/S0006-3223(03)00010-6 405
Goldsmith, H. H., & Rothbart, M. K. (1999). Laboratory Temperament Assessment Battery, Prelocomotor Version 3.1. University of Wisconsin.
Granger, D. A., Serbin, L. A., Schwartzman, A., Lehoux, P., Cooperman, J., & Ikeda, S. (1998). Children's salivary cortisol, internalising behaviour problems, and family environment: Results from the Concordia Longitudinal Risk Project. International Journal of Behavioral Development, 22(4), 707–728.
Granger, D. A., & Taylor, M. K. (Eds.). (2020). Salivary bioscience: foundations of interdisciplinary saliva research and applications. Springer Nature.
Hagan, M. J., Roubinov, D. S., Boyce, W. T., & Bush, N. R. (2020). Associations between multisystem stress reactivity and peer nominated aggression in early childhood vary by sex. Development and Psychopathology, 32(5), 1888–1898. https://doi.org/10.1017/S0954579420001406
Hay, D. F. (2016). The early development of human aggression. Child Development Perspectives, 11(2), 102–106. https://doi-org.vu-nl.idm.oclc.org/10.1111/cdep.12220
Hill-Soderlund, A. L., Holochwost, S. J., Willoughby, M. T., Granger, D. A., Gariépy, J. L., Mills-Koonce, W. R., & Cox, M. J. (2015). The developmental course of salivary alpha-amylase and cortisol from 12 to 36 months: Relations with early poverty and later behavior problems. Psychoneuroendocrinology, 52, 311–323.
Jung, T., & Wickrama, K. A. S. (2008). An introduction to latent class growth analysis and growth mixture modeling. Social and Personality Psychology Compass, 2(1), 302–317. https://doi.org/10.1111/j.1751-9004.2007.00054.x
Lin, B., Kidwell, M. C., Kerig, P. K., Crowell, S. E., & Fortuna, A. J. (2020). Profiles of autonomic stress responsivity in a sample of justice-involved youth: Associations with childhood trauma exposure and emotional and behavioral functioning. Developmental Psychobiology, 63(2), 206–225. https://doi.org/10.1002/dev.21968
Little, R. J. (1988). A test of missing completely at random for multivariate data with missing values. Journal of the American statistical Association, 83(404), 1198–1202. https://doi.org/10.1080/01621459.1988.10478722
Lorber, M. F. (2004). Psychophysiology of aggression, psychopathy, and conduct problems: a metaanalysis. Psychological Bulletin, 130(4), 531–552. https://doi.org/10.1037/0033-2909.130.4.531
Lorber, M. F., Del Vecchio, T., & Slep, A. M. S. (2015). The emergence and evolution of infant externalizing behavior. Development and Psychopathology, 27(3), 663–680. https://doi.org/10.1017/S0954579414000923
Lorber, M. F., Del Vecchio, T. D., & Slep, A. M. S. (2018). The development of individual physically aggressive behaviors from infancy to toddlerhood. Developmental Psychology, 54(4), 601–612. https://doi.org/10.1037/dev0000450.supp
Matthews, K. A., Salomon, K., Kenyon, K., & Allen, M. T. (2002). Stability of children's and adolescents' hemodynamic responses to psychological challenge: A three-year longitudinal study of a multiethnic cohort of boys and girls. Psychophysiology, 39(6), 826–834. https://doi.org/10.1111/1469-8986.3960826
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840(1), 33–44. https://doi.org/10.1111/j.1749-6632.1998.tb09546.x
Mesman, J., Alink, L. R. A., Van Zeijl, J., Stolk, M. N., Bakermans-Kranenburg, M. J., Van IJzendoorn, M. H., Juffer, F., & Koot, H. M. (2008). Observation of early childhood physical aggression: A psychometric study of the system for coding early physical aggression. Aggressive Behavior, 34(5), 539–552. https://doi.org/10.1002/ab.20267 406
Moore, G. A. (2009). Infants’ and mothers’ vagal reactivity in response to anger. Journal of Child Psychology and Psychiatry, 50(11), 1392–1400. https://doi.org/10.1111/j.1469-7610.2009.02171.x
Nagy, T., Van Lien, R., Willemsen, G., Proctor, G., Efting, M., Fülöp, M., Bárdos, G., Veerman, E. C. I., & Bosch, J. A. (2015). A fluid response: Alpha-amylase reactions to acute laboratory stress are related to sample timing and saliva flow rate. Biological Psychology, 109, 111–119. https://doi.org/10.1016/j.biopsycho.2015.04.012
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(4), 486–496.
Ortiz, J., & Raine, A. (2004). Heart rate level and antisocial behavior in children and adolescents: A meta-analysis. Journal of the American Academy of Child & Adolescent Psychiatry, 43(2), 154–162. https://doi.org/10.1097/00004583-200402000-00010
Patriquin, M. A., Lorenzi, J., Scarpa, A., Calkins, S. D., & Bell, M. A. (2015). Broad implications for respiratory sinus arrhythmia development: Associations with childhood symptoms of psychopathology in a community sample. Developmental Psychobiology, 57(1), 120–130. https://doi.org/10.1002/dev.21269
Peckins, M. K., Susman, E. J., Negriff, S., Noll, J., & Trickett, P. K. (2015). Cortisol profiles: A test for adaptive calibration of the stress response system in maltreated and nonmaltreated youth. Development and Psychopathology, 27(4pt2), 1461–1470. https://doi.org/10.1017/S0954579415000875
Porges, S. W. (2007). A phylogenetic journey through the vague and ambiguous Xth cranial nerve: A commentary on contemporary heart rate variability research. Biological Psychology, 74(2), 301-307. https://doi.org/10.1016/j.biopsycho.2006.08.007
Porges, S. W., Doussard-Roosevelt, J. A., & Maiti, A. K. (1994). Vagal tone and the physiological regulation of emotion. Monographs of the Society for Research in Child Development, 59(2-3), 167–186.
Quas, J. A., Yim, I. S., Oberlander, T. F., Nordstokke, D., Essex, M. J., Armstrong, J. M., Bush, N., Obradović, J., & Boyce, W. T. (2014). The symphonic structure of childhood stress reactivity: Patterns of sympathetic, parasympathetic, and adrenocortical responses to psychological challenge. Development and Psychopathology, 26(4pt1), 963–982. https://doi.org/10.1017/S0954579414000480
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Raine, A., Venables, P. H., & Mednick, S. A. (1997). Low resting heart rate at age 3 years predisposes to aggression at age 11 years: Evidence from the Mauritius Child Health Project. Journal of the American Academy of Child & Adolescent Psychiatry, 36(10), 1457–1464. https://doi.org/10.1097/00004583-199710000-00029
Reiter, J. P. (2007). Small-sample degrees of freedom for multi-component significance tests with multiple imputation for missing data. Biometrika, 94(2), 502–508. https://doi.org/10.1093/biomet/asm028
Robitzsch, A., & Grund, S. (2021). miceadds: Some Additional Multiple Imputation Functions, Especially for 'mice'. R package version 3.12-9. https://CRAN.R-project.org/package=miceadds
Rosenberg, J. M., Beymer, P. N., Anderson, D. J., Van Lissa, C. J., & Schmidt, J. A. (2018). tidyLPA: An R package to easily carry out Latent Profile Analysis (LPA) using open-source or commercial software. Journal of Open Source Software, 3(30), 978. https://doi.org/10.21105/joss.00978
Roubinov, D. S., Boyce, W. T., Lee, M. R., & Bush, N. R. (2020). Evidence for discrete profiles of children’s physiological activity across three neurobiological system and their transitions over time. Developmental Science, 24(1), 1–17. https://doi.org/10.1111/desc.12989 407
Rubin, D. B. (1988). An overview of multiple imputation. In Proceedings of the survey research methods section of the American statistical association (pp. 79-84). Citeseer.
Rudd, K. L., Bush, N. R., Alkon, A., & Roubinov, D. S. (2021). Identifying profiles of multisystem physiological activity across early childhood: Examining developmental shifts and associations with stress and internalizing problems. Psychoneuroendocrinology, 128, 105196. https://doi.org/10.1016/j.psyneuen.2021.105196
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1), 55–89. https://doi.org/10.1210/edrv.21.1.0389
Sherwood, A., Allen, M. T., Fahrenbert, J., Kelsey, R. M., Lovallo, W. R., & van Doornen, L. J. P. (1990). Committee report: Methodological guidelines for impedance cardiography. Psychophysiology, 27(1), 1–23. https://doi.org/10.1111/j.1469-8986.1990.tb02171.x
Shirtcliff, E. A., Granger, D. A., Booth, A., & Johnson, D. (2005). Low salivary cortisol levels and externalizing behavior problems in youth. Development and Psychopathology, 17(1), 167–184.
Sijtsema, J. J., Shoulberg, E. K., & Murray-Close, D. (2011). Physiological reactivity and different forms of aggression in girls: Moderating roles of rejection sensitivity and peer rejection. Biological Psychology, 86(3), 181–192. https://doi.org/10.1016/j.biopsycho.2010.11.007
Smaling, H. J. A., Suurland, J., Huijbregts, S. C. J., Van der Heijden, K. B., Van Goozen, S., & Swaab, H. (2017). The Mother-Infant Neurodevelopment Study (MINDS)–Leiden: Background, design and study population. Maternal reflective functioning: Influence on parenting practices and the early development of externalizing behavior, 29.
Snoek, H., Van Goozen, S. H. M., Matthys, W., Buitelaar, J. K., & Van Engeland, H. (2004). Stress responsivity in children with externalizing behavior disorders. Development and Psychopathology, 16(2), 389–406.
Spurk, D., Hirschi, A., Wang, M., Valero, D., & Kauffeld, S. (2020). Latent profile analysis: A review and “how to” guide of its application within vocational behavior research. Journal of Vocational Behavior, 120, 103445. https://doi.org/10.1016/j.jvb.2020.103445
Suurland, J., Van der Heijden, K. B., Huijbregts, S.C.J., Van Goozen, S. H. M., & Swaab, H. (2017). Interaction between prenatal risk and infant parasympathetic and sympathetic stress reactivity predicts early aggression. Biological Psychology, 128, 98-104. https://doi: 10.1016/j.biopsycho.2017.07.005.
Tremblay, R. E. (2004). Decade of behavior distinguished lecture: Development of physical aggression during infancy. Infant Mental Health Journal, 25(5), 399–407. https://doi.org/10.1002/imhj.20015
Tremblay, R. E., Nagin, D. S., Seguin, J. R., Zoccolillo, M., Zelazo, P. D., Boivin, M., Pérusse, D. & Japel, C. (2004). Physical aggression during early childhood: Trajectories and predictors. Pediatrics, 114(1), E43–E50. https://doi.org/10.1542/peds.114.1.e43
Van Adrichem, D.S., Huijbregts, S.C.J., Van der Heijden, K.B., Van Goozen, S.H.M., & Swaab, H. (2020). Aggressive behavior during toddlerhood: interrelated effects of Prenatal risk factors, negative affect and cognition. Child Neuropsychology, 26, 982-1004. https://doi: 10.1080/09297049.2020.1769582
Van Buuren, S., & Groothuis-Oudshoorn, K. (2011). mice: Multivariate Imputation by Chained Equations in R. Journal of Statistical Software, 45(3), 1–67. https://www.jstatsoft.org/v45/i03/
Van Ginkel, J. R., & Kroonenberg, P. M. (2014). Analysis of variance of multiply imputed data. Multivariate Behavioral Research, 49(1), 78–91. https://doi.org/10.1080/00273171.2013.855890 408
Van Ginkel, J. R., Linting, M., Rippe, R. C., & van der Voort, A. (2020). Rebutting existing misconceptions about multiple imputation as a method for handling missing data. Journal of Personality Assessment, 102(3), 297–308. https://doi.org/10.1080/00223891.2018.1530680
Van Goozen, S. H. M., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The evidence for a neurobiological model of childhood antisocial behavior. Psychological Bulletin, 133(1), 149–182. https://doi.org/10.1037/0033-2909.133.1.149
Willemsen, G. H. M., De Geus, E. J. C., Klaver, C. H. A. M., Van Doornen, L. J. P., & Carroll, D. (1996). Ambulatory monitoring of the impedance cardiogram. Psychophysiology, 33(2), 184–193. https://doi.org/10.1111/j.1469-8986.1996.tb02122.x
Xu, Y., Raine, A., Yu, L., & Krieg, A. (2014). Resting heart rate, vagal tone, and reactive and proactive aggression in Chinese children. Journal of Abnormal Child Psychology, 42(3), 501–514. https://doi.org/10.1007/s10802-013-9792-2
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Elja E. J. Meijer, Stephan C. J. Huijbregts, Stephanie H. M. Van Goozen, Hanna Swaab
This work is licensed under a Creative Commons Attribution 4.0 International License.
