Adversity in preschool-aged children: Effects on salivary interleukin-1β

Development and Psychopathology

Volumn 27, Issue 2, 2015, Pages 567-576

  Tyrka, Audrey R ^a,b   Parade, Stephanie H ^b,c   Valentine, Thomas R ^a   Eslinger, Nicole M ^a   Seifer, Ronald ^b,c  

^a BUTLER HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

^c E P BRADLEY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; INTERLEUKIN 1BETA;

CHEMISTRY; FEMALE; HUMAN; INFLAMMATION; LIFE EVENT; MALE; MENTAL STRESS; METABOLISM; PRESCHOOL CHILD; SALIVA; SOCIAL ENVIRONMENT;

BIOMARKERS; C-REACTIVE PROTEIN; CHILD, PRESCHOOL; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; LIFE CHANGE EVENTS; MALE; SALIVA; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL;

EID: 84928953591     PISSN: 09545794     EISSN: 14692198     Source Type: Journal    
DOI: 10.1017/S0954579415000164     Document Type: Article

References (95)

1. Abidin, R. R. (1995). Parenting Stress Index: Professional manual. Odessa, FL: Psychological Assessment Resources.
2. American Dental Association Division of Communications, Journal of the American Dental Association, ADA Council on Scientific Affairs. (2005). Tooth eruption: The primary teeth. Journal of the American Dental Association, 136, 1619.
3. American Dental Association Division of Communications, Journal of the American Dental Association, ADA Council on Scientific Affairs. (2006). Tooth eruption: The permanent teeth. Journal of the American Dental Association, 137, 127.
4. Appleton, A. A., Buka, S. L., McCormick, M. C., Koenen, K. C., Loucks, E. B., Kubzansky, L. D. (2012). The association between childhood emotional functioning and adulthood inflammation is modified by early-life socioeconomic status. Health Psychology, 31, 413-422.
5. Appleyard, K., Egeland, B., van Dulmen, M. H., Sroufe, L. A. (2005). When more is not better: The role of cumulative risk in child behavior outcomes. Journal of Child Psychology and Psychiatry and Allied Disciplines, 46, 235-245.
6. Araujo, D. M., Cotman, C.W. (1995). Differential effects of interleukin-1 beta and interleukin-2 on glia and hippocampal neurons in culture. International Journal of Developmental Neuroscience, 13, 201-212.
7. Bailey, M. T., Kinsey, S. G., Padgett, D. A., Sheridan, J. F., Leblebicioglu, B. (2009). Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b\+ cells. Physiology & Behavior, 98, 351-358.
8. Baker D. G., Nievergelt, C. M., O'Connor, D. T. (2012). Biomarkers of PTSD: Neuropeptides and immune signaling. Neuropharmacology 62 663-673.
9. Barkho, B. Z., Song, H., Aimone, J. B., Smrt, R. D., Kuwabara, T., Nakashima, K., et al. (2006). Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells and Development, 15, 407-421.
10. Barnett, D., Manly, J. T., Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In D. Cicchetti & S. L. Toth (Eds.), Child abuse, child development and social policy (pp. 7-73). Norwood, NJ: Ablex.
11. Bernardino, L., Agasse, F., Silva, B., Ferreira, R., Grade, S., Malva, J. O. (2008). Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells, 26, 2361-2371.
12. Bertone-Johnson, E. R., Whitcomb, B.W., Missmer, S. A., Karlson, E.W., Rich-Edwards, J. W. (2012). Inflammation and early-life abuse in women. American Journal of Preventive Medicine, 43, 611-620.
13. Bhasin, M. K., Dusek, J. A., Chang, B. H., Joseph, M. G., Denninger, J. W., Fricchione, G. L., et al. (2013) Relaxation response induces temporal transcriptome changes in energy metabolism, insulin secretion and inflammatory pathways. PLOS ONE, 8, 1-13.
14. Brody, G. H., Yu, T., Chen, Y. F., Kogan, S. M., Evans, G. W., Windle, M., et al. (2013). Supportive family environments, genes that confer sensitivity, and allostatic load among rural African American emerging adults: A prospective analysis. Journal of Family Psychology, 27, 22-29.
15. Bronfenbrenner, U. (1977). Doing your own thing-Our undoing. Child Psychiatry and Human Development, 8, 3-10.
16. Brown, D.W., Anda, R. F., Tiemeier, H., Felitti, V. J., Edwards, V. J., Croft, J. B., et al. (2009). Adverse childhood experiences and the risk of premature mortality. American Journal of Preventive Medicine, 37, 389-396.
17. Brown, G. R., Anderson, B. (1991). Psychiatric morbidity in adult inpatients with childhood histories of sexual and physical abuse. American Journal of Psychiatry, 148, 55-61.
18. Broyles, S. T., Staiano, A. E., Drazba, K. T., Gupta, A. K., Sothern, M., Katzmarzyk, P. T. (2012). Elevated C-reactive protein in children from risky neighborhoods: Evidence for a stress pathway linking neighborhoods and inflammation in children. PLOS ONE, 7, e45419.
19. Brydon, L., Edwards, S., Jia, H., Mohamed-Ali, V., Zachary, I., Martin, J. F., et al. (2005). Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain, Behavior, and Immunity, 19, 540-546.
20. Bryer, J. B., Nelson, B. A., Miller, J. B., Krol, P. A. (1987). Childhood sexual and physical abuse as factors in adult psychiatric illness. American Journal of Psychiatry, 144, 1426-1430.
21. Burns, B. J., Phillips, S. D., Wagner, H. R., Barth, R. P., Kolko, D. J., Campbell, Y., et al. (2004). Mental health need and access to mental health services by youths involved with childwelfare:Anational survey. Journal of the American Academy of Child & Adolescent Psychiatry, 43, 960-970.
22. Byrne, M. L., O'Brien-Simpson, N. M., Reynolds, E. C., Walsh, K. A., Laughton, K., Waloszek, J. M., et al. (2013). Acute phase protein and cytokine levels in serum and saliva: A comparison of detectable levels and correlations in a depressed and healthy adolescent sample. Brain, Behavior, and Immunity, 34, 164-175.
23. Cacci, E., Claasen, J. H., Kokaia, Z. (2005). Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. Journal of Neuroscience Research, 80, 789-797.
24. Carpenter, L. L., Gawuga, C. E., Tyrka, A. R., Lee, J. K., Anderson, G. M., Price, L. H. (2010). Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology, 35, 2617-2623.
25. Carpenter, L. L., Gawuga, C. E., Tyrka, A. R., Price, L. H. (2012). C-reactive protein, early life stress, and well-being in healthy adults. Acta Psychiatrica Scandinavica, 126, 402-410.
26. Caso, J. R., Moro, M. A., Lorenzo, P., Lizasoain, I., Leza, J. C. (2007). Involvement of IL-1beta in acute stress-induced worsening of cerebral ischaemia in rats. European Neuropsychopharmacology, 17, 600-607.
27. Chen, E., Miller, G. E., Kobor, M. S., Cole, S.W. (2011). Maternal warmth buffers the effects of low early-life socioeconomic status on pro-inflammatory signaling in adulthood. Molecular Psychiatry, 16, 729-737.
28. Cicchetti, D. (2013). Annual Research Review: Resilient functioning in maltreated children-Past, present, and future perspectives. Journal of Child Psychology and Psychiatry and Allied Disciplines, 54, 402-422.
29. Cicchetti, D., Lynch, M. (1993). Toward an ecological/transactional model of community violence and child maltreatment: Consequences for children's development. Psychiatry, 56, 96-118.
30. Coelho, R., Viola, T.W., Walss-Bass, C., Brietzke, E., Grassi-Oliveira, R. (2013). Childhood maltreatment and inflammatory markers: A systematic review. Acta Psychiatrica Scandinavica. Advance online publication.
31. Cook, D. G., Mendall, M. A., Whincup, P. H., Carey, I. M., Ballam, L., Morris, J. E., et al. (2000). C-reactive protein concentration in children: Relationship to adiposity and other cardiovascular risk factors. Atherosclerosis, 149, 139-150.
32. Danese, A., Caspi, A., Williams, B., Ambler, A., Sugden, K., Mika, J., et al. (2011). Biological embedding of stress through inflammation processes in childhood. Molecular Psychiatry, 16, 244-246.
33. Danese, A., Moffitt, T. E., Pariante, C. M., Ambler, A., Poulton, R., Caspi, A. (2008). Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Archives of General Psychiatry, 65, 409-415.
34. Danese, A., Pariante, C. M., Caspi, A., Taylor, A., Poulton, R. (2007). Childhood maltreatment predicts adult inflammation in a life-course study. Proceedings of the National Academy of Sciences, 104, 1319-1324.
35. Dantzer, R. (2009). Cytokine, sickness behavior, and depression. Immunology and Allergy Clinics of North America, 29, 247-264.
36. Dixon, D., Meng, H., Goldberg, R., Schneiderman, N., Delamater, A. (2009). Stress and body mass index each contributes independently to tumor necrosis factor-alpha production in prepubescent Latino children. Journal of Pediatric Nursing, 24, 378-388.
37. Dowd, J. B., Zajacova, A., Aiello, A. E. (2010). Predictors of inflammation in U.S. children aged 3-16 years. American Journal of Preventive Medicine, 39, 314-320.
38. Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E. K., et al. (2010). A meta-analysis of cytokines in major depression. Biological Psychiatry, 67, 446-457.
39. Gaskin, D. J., Thorpe, R. J., Jr., McGinty, E. E., Bower, K., Rohde, C., Young, J. H., et al. (2013). Disparities in diabetes: The nexus of race, poverty, and place. American Journal of Public Health. Advance online publication.
40. Gimeno, D., Ferrie, J. E., Elovainio, M., Pulkki-Raback, L., Keltikangas-Jarvinen, L., Eklund, C., et al. (2008). When do social inequalities in C-reactive protein start? A life course perspective from conception to adulthood in the Cardiovascular Risk in Young Finns Study. International Journal of Epidemiology, 37, 290-298.
41. Gola, H., Engler, H., Sommershof, A., Adenauer, H., Kolassa, S., Schedlowski, M., et al. (2013). Posttraumatic stress disorder is associated with an enhanced spontaneous production of pro-inflammatory cytokines by peripheral blood mononuclear cells. BMC Psychiatry, 13, 40.
42. Hartwell, K. J., Moran-Santa Maria, M. M., Twal, W. O., Shaftman, S., De-Santis, S. M., McRae-Clark, A. L., et al. (2013). Association of elevated cytokines with childhood adversity in a sample of healthy adults. Journal of Psychiatric Research, 47, 604-610.
43. Herberth, G., Weber, A., Roder, S., Elvers, H. D., Kramer, U., Schins, R. P., et al. (2008). Relation between stressful life events, neuropeptides and cytokines: Results from the LISA birth cohort study. Pediatric Allergy and Immunology, 19, 722-729.
44. Hiles, S. A., Baker, A. L., de Malmanche, T., Attia, J. (2012). A meta-analysis of differences in IL-6 and IL-10 between people with and without depression: Exploring the causes of heterogeneity. Brain, Behavior, and Immunity, 26, 1180-1188.
45. Howe, L. D., Galobardes, B., Sattar, N., Hingorani, A. D., Deanfield, J., Ness, A. R., et al. (2010). Are there socioeconomic inequalities in cardiovascular risk factors in childhood, and are they mediated by adiposity? Findings from a prospective cohort study. International Journal of Obesity (London), 34, 1149-1159.
46. Kohman, R. A., Rhodes, J. S. (2013). Neurogenesis, inflammation and behavior. Brain, Behavior, and Immunity, 27, 22-32.
47. Koinis-Mitchell, D., McQuaid, E. L., Seifer, R., Kopel, S. J., Esteban, C., Canino, G., et al. (2007). Multiple urban and asthma-related risks and their association with asthma morbidity in children. Journal of Pediatric Psychology, 32, 582-595.
48. Koo, J. W., Duman, R. S. (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proceedings of the National Academy of Sciences, 105, 751-756.
49. Krishnadas, R., McLean, J., Batty, G. D., Burns, H., Deans, K. A., Ford, I., et al. (2013). Socioeconomic deprivation and cortical morphology: Psychological, social, and biological determinants of ill health study. Psychosomatic Medicine, 75, 616-623.
50. Lacy, P., Stow, J. L. (2011). Cytokine release from innate immune cells: Association with diverse membrane trafficking pathways. Blood, 118, 9-18.
51. Liu, Y., Ho, R. C., Mak, A. (2012). Interleukin (IL)-6, tumour necrosis factor alpha (TNF-alpha) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: A meta-analysis and meta-regression. Journal of Affective Disorders, 139, 230-239.
52. Ludwig, J., Sanbonmatsu, L., Gennetian, L., Adam, E., Duncan, G. J., Katz, L. F., et al. (2011). Neighborhoods, obesity, and diabetes-A randomized social experiment. New England Journal of Medicine, 365, 1509-1519.
53. Marin, T. J., Martin, T. M., Blackwell, E., Stetler, C., Miller, G. E. (2007). Differentiating the impact of episodic and chronic stressors on hypothalamic-pituitary-adrenocortical axis regulation in young women. Health Psychology, 26, 447-455.
54. Mastrolonardo, M., Alicino, D., Zefferino, R., Pasquini, P., Picardi, A. (2007). Effect of psychological stress on salivary interleukin-1beta in psoriasis. Archives of Medical Research, 38, 206-211.
55. Matthews, K. A., Chang, Y. F., Thurston, R. C., Bromberger, J. T. (2013). Child abuse is related to inflammation in mid-life women: Role of obesity.
56. Brain, Behavior, and Immunity. Advance online publication. McDade, T. W., Leonard, W. R., Burhop, J., Reyes-Garcia, V., Vadez, V., Huanca, T., et al. (2005). Predictors of C-reactive protein in Tsimane' 2-to 15-year-olds in lowland Bolivia. American Journal of Physical Anthropology, 128, 906-913.
57. Megson, E., Fitzsimmons, T., Dharmapatni, K., Bartold, P. M. (2010). Creactive protein in gingival crevicular fluid may be indicative of systemic inflammation. Journal of Clinical Periodontology, 37, 797-804.
58. Miller, G. E., Chen, E. (2010). Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychological Science, 21, 848-856.
59. Miller, G. E., Chen, E., Fok, A. K., Walker, H., Lim, A., Nicholls, E. F., et al. (2009). Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proceedings of the National Academy of Sciences, 106, 14716-14721.
60. Miller, G. E., Cole, S. W. (2012). Clustering of depression and inflammation in adolescents previously exposed to childhood adversity. Biological Psychiatry, 72, 34-40.
61. Mills, N. T., Scott, J. G., Wray, N. R., Cohen-Woods, S., Baune, B. T. (2013). Research review: The role of cytokines in depression in adolescents: A systematic review. Journal of Child Psychology and Psychiatry and Allied Disciplines, 54, 816-835.
62. Monje, M. L., Toda, H., Palmer, T. D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science, 302, 1760-1765.
63. Murasko, J. E. (2008). Male-female differences in the association between socioeconomic status and atherosclerotic risk in adolescents. Social Science and Medicine, 67, 1889-1897.
64. Nguyen, K. T., Deak, T., Owens, S. M., Kohno, T., Fleshner, M., Watkins, L. R., et al. (1998). Exposure to acute stress induces brain interleukin-1beta protein in the rat. Journal of Neuroscience, 18, 2239-2246.
65. Nikas, J. B. (2013). Inflammation and immune system activation in aging: A mathematical approach. Scientific Reports, 3, 3254.
66. O'Donovan, A., Sun, B., Cole, S., Rempel, H., Lenoci, M., Pulliam, L., et al. (2011). Transcriptional control of monocyte gene expression in post-traumatic stress disorder. Disease Markers, 30, 123-132.
67. Ouellet-Morin, I., Danese, A., Williams, B., Arseneault, L. (2011). Validation of a high-sensitivity assay for C-reactive protein in human saliva. Brain, Behavior, and Immunity, 25, 640-646.
68. Out, D., Hall, R. J., Granger, D. A., Page, G. G., Woods, S. J. (2012). Assessing salivary C-reactive protein: Longitudinal associations with systemic inflammation and cardiovascular disease risk in women exposed to intimate partner violence. Brain, Behavior, and Immunity, 26, 543-551.
69. Pace, T.W., Wingenfeld, K., Schmidt, I., Meinlschmidt, G., Hellhammer, D. H., Heim, C. M. (2012). Increased peripheral NF-kappaB pathway activity in women with childhood abuse-related posttraumatic stress disorder. Brain, Behavior, and Immunity, 26, 13-17.
70. Pandey, G.N., Rizavi, H. S., Ren, X., Fareed, J., Hoppensteadt, D. A., Roberts, R. C., et al. (2012). Proinflammatory cytokines in the prefrontal cortex of teenage suicide victims. Journal of Psychiatric Research, 46, 57-63.
71. Phillips, A. C., Batty, G. D., van Zanten, J. J., Mortensen, L. H., Deary, I. J., Calvin, C. M., et al. (2011). Cognitive ability in early adulthood is associated with systemic inflammation in middle age: The Vietnam experience study. Brain, Behavior, and Immunity, 25, 298-301.
72. Pollitt, R. A., Kaufman, J. S., Rose, K. M., Diez-Roux, A. V., Zeng, D., Heiss, G. (2007). Early-life and adult socioeconomic status and inflammatory risk markers in adulthood. European Journal of Epidemiology, 22, 55-66
73. Porterfield, V. M., Gabella, K. M., Simmons, M. A., Johnson, J. D. (2012). Repeated stressor exposure regionally enhances beta-adrenergic receptormediated brain IL-1beta production. Brain, Behavior, and Immunity, 26, 1249-1255.
74. Price, L. H., Kao, H. T., Burgers, D. E., Carpenter, L. L., Tyrka, A. R. (2013). Telomeres and early-life stress: An overview. Biological Psychiatry, 73, 15-23.
75. Riis, J. L., Out, D., Dorn, L. D., Beal, S. J., Denson, L. A., Pabst, S., et al. (2013). Salivary cytokines in healthy adolescent girls: Intercorrelations, stability, and associations with serum cytokines, age, and pubertal stage. Developmental Psychobiology. Advance online publication.
76. Robles, T. F., Glaser, R., Kiecolt-Glaser, J. K. (2005). Out of balance: A new look at chronic stress, depression, and immunity. Current Directions in Psychological Science, 14, 111-115.
77. Rooks, C., Veledar, E., Goldberg, J., Bremner, J. D., Vaccarino, V. (2012). Early trauma and inflammation: Role of familial factors in a study of twins. Psychosomatic Medicine, 74, 146-152.
78. Rosenkranz, M. A., Davidson, R. J., Maccoon, D. G., Sheridan, J. F., Kalin, N. H., Lutz, A. (2013). A comparison of mindfulness-based stress reduction and an active control in modulation of neurogenic inflammation. Brain, Behavior, and Immunity, 27, 174-184.
79. Sameroff, A. J., Seifer, R., Baldwin, A., Baldwin, C. (1993). Stability of intelligence from preschool to adolescence: The influence of social and family risk factors. Child Development, 64, 80-97.
80. Scheeringa, M. S., Haslett, N. (2010). The reliability and criterion validity of the Diagnostic Infant and Preschool Assessment: A new diagnostic instrument for young children. Child Psychiatry and Human Development, 41, 299-312.
81. Shonkoff, J. P., Garner, A. S. (2012). Committee on Psychosocial Aspects of Child and Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics: The lifelong effects of early childhood adversity and toxic stress. Pediatrics, 129, e232-e246.
82. Slopen, N., Kubzansky, L. D., Koenen, K. C. (2013). Internalizing and externalizing behaviors predict elevated inflammatory markers in childhood. Psychoneuroendocrinology, 38, 2854-2862.
83. Slopen, N., Kubzansky, L. D., McLaughlin, K. A., Koenen, K. C. (2013). Childhood adversity and inflammatory processes in youth: A prospective study. Psychoneuroendocrinology, 38, 188-200.
84. Steptoe, A., Hamer, M., Chida, Y. (2007). The effects of acute psychological stress on circulating inflammatory factors in humans: A review and meta-analysis. Brain, Behavior, and Immunity, 21, 901-912.
85. Teunissen, C. E., van Boxtel, M. P., Bosma, H., Bosmans, E., Delanghe, J., De Bruijn, C., et al. (2003). Inflammation markers in relation to cognition in a healthy aging population. Journal of Neuroimmunology, 134, 142-150.
86. Thomas, N. E., Cooper, S. M., Williams, S. R., Baker, J. S., Davies, B. (2005). Fibrinogen, homocyst(e)ine, and C-reactive protein concentrations relative to sex and socioeconomic status in British young people. American Journal of Human Biology, 17, 809-813.
87. Tyrka, A. R., Burgers, D. E., Philip, N. S., Price, L. H., Carpenter, L. L. (2013). The neurobiological correlates of childhood adversity and implications for treatment. Acta Psychiatrica Scandinavica, 128, 434-437.
88. Udina, M., Castellvi, P., Moreno-Espana, J., Navines, R., Valdes, M., Forns, X., et al. (2012). Interferon-induced depression in chronic hepatitis C: A systematic review and meta-analysis. Journal of Clinical Psychiatry, 73, 1128-1138.
89. Valkanova, V., Ebmeier, K. P., Allan, C. L. (2013). CRP, IL-6 and depression: A systematic reviewand meta-analysis of longitudinal studies. Journal of Affective Disorders, 150, 736-744.
90. Williamson, S., Munro, C., Pickler, R., Grap, M. J., Elswick, R. K., Jr. (2012). Comparison of biomarkers in blood and saliva in healthy adults. Nursing Research and Practice, 2012, 246178.
91. Wright, C. B., Sacco, R. L., Rundek, T., Delman, J., Rabbani, L., Elkind, M. (2006). Interleukin-6 is associated with cognitive function: The Northern Manhattan Study. Journal of Stroke and Cerebrovascular Diseases, 15, 34-38.
92. Yaffe, K., Lindquist, K., Penninx, B. W., Simonsick, E. M., Pahor, M., Kritchevsky, S., et al. (2003). Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology, 61, 76-80.
93. Yamakawa, K., Matsunaga, M., Isowa, T., Kimura, K., Kasugai, K., Yoneda, M., et al. (2009). Transient responses of inflammatory cytokines in acute stress. Biological Psychology, 82, 25-32.
94. You, Z., Luo, C., Zhang, W., Chen, Y., He, J., Zhao, Q., et al. (2011). Proand anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: Involvement in depression. Behavioural Brain Research, 225, 135-141.
95. Zunszain, P. A., Anacker, C., Cattaneo, A., Choudhury, S., Musaelyan, K., Myint, A. M., et al. (2012). Interleukin-1beta: A new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology, 37, 939-949.