Adiposity moderates links from early adversity and depressive symptoms to inflammatory reactivity to acute stress during late adolescence

Brain, Behavior, and Immunity

Volumn 66, Issue , 2017, Pages 146-155

  Chiang, Jessica J ^a   Bower, Julienne E ^b   Irwin, Michael R ^b   Taylor, Shelley E ^b   Fuligni, Andrew J ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adolescents; Body mass index; Depressive symptoms; Early life stress; IL 6; Risky families; Waist circumference

Indexed keywords

HYDROCORTISONE; INTERLEUKIN 6;

ACUTE STRESS; ADOLESCENCE; ADULT; ARTICLE; BODY HEIGHT; BODY MASS; BODY WEIGHT; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; EARLY LIFE STRESS; FEMALE; FOLLOW UP; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RETROSPECTIVE STUDY; WAIST CIRCUMFERENCE; YOUNG ADULT; ADOLESCENT; BLOOD; COMPLICATION; MENTAL STRESS;

ADIPOSITY; ADOLESCENT; ADULT; DEPRESSION; FEMALE; HUMANS; HYDROCORTISONE; INFLAMMATION; INTERLEUKIN-6; MALE; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 85023600013     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2017.06.015     Document Type: Article

References (94)

1. Avenevoli, S., Swendsen, J., He, J.P., Burstein, M., Merikangas, K.R., Major depression in the National Comorbidity Survey-Adolescent Supplement: prevalence, correlates, and treatment. J. Am. Acad. Child Adolesc. Psychiatry 54:1 (2015), 37–44.
2. Bauer, K.W., Marcus, M.D., Ogden, C.L., Foster, G.D., Cardio-metabolic risk screening among adolescents: understanding the utility of body mass index, waist circumference and waist to height ratio. Pediatr. Obesity 10:5 (2015), 329–337.
3. Black, P.H., The inflammatory response is an integral part of the stress response: implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain Behav. Immun. 17:5 (2003), 350–364.
4. Black, P.H., The inflammatory consequences of psychologic stress: relationship to insulin resistance, obesity, atherosclerosis and diabetes mellitus, type II. Med. Hypotheses 67:4 (2006), 879–891.
5. Blakemore, S.J., Mills, K.L., Is adolescence a sensitive period for sociocultural processing?. Annu. Rev. Psychol. 65 (2014), 187–207.
6. Brown, D.W., Anda, R.F., Tiemeier, H., Felitti, V.J., Edwards, V.J., Croft, J.B., Giles, W.H., Adverse childhood experiences and the risk of premature mortality. Am. J. Prev. Med. 37:5 (2009), 389–396.
7. Brydon, L., Steptoe, A., Stress-induced increases in interleukin-6 and fibrinogen predict ambulatory blood pressure at 3-year follow-up. J. Hypertens. 23:5 (2005), 1001–1007.
8. Burke, H.M., Davis, M.C., Otte, C., Mohr, D.C., Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30:9 (2005), 846–856.
9. Carpenter, L.L., Gawuga, C.E., Tyrka, A.R., Lee, J.K., Anderson, G.M., Price, L.H., Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology 35:13 (2010), 2617–2623.
10. Carroll, J.E., Low, C.A., Prather, A.A., Cohen, S., Fury, J.M., Ross, D.C., Marsland, A.L., Negative affective responses to a speech task predict changes in interleukin (IL)-6. Brain Behav. Immun. 25:2 (2011), 232–238.
11. Chiang, J.J., Bower, J.E., Almeida, D.M., Irwin, M.R., Seeman, T., Fuligni, A.J., Socioeconomic status, daily affective and social experiences, and inflammation during adolescence. Psychosom. Med. 77:3 (2015), 256–266.
12. Chiang, J.J., Bower, J.E., Taylor, S.E., Early adversity, neural development, and inflammation. Dev. Psychobiol. 57:8 (2015), 887–907.
13. Chiang, J.J., Tsai, K.M., Park, H., Bower, J.E., Almeida, D.M., Dahl, R.E., Fuligni, A.J., Daily family stress and HPA axis functioning during adolescence: the moderating role of sleep. Psychoneuroendocrinology 71 (2016), 43–53.
14. Cook, S., Weitzman, M., Auinger, P., Nguyen, M., Dietz, W.H., Prevalence of a metabolic syndrome phenotype in adolescents: findings from the third National Health and Nutrition Examination Survey, 1988–1994. Arch. Pediatr. Adolesc. Med. 157:8 (2003), 821–827.
15. Copeland, W.E., Shanahan, L., Worthman, C., Angold, A., Costello, E.J., Cumulative depression episodes predict later C-reactive protein levels: a prospective analyses. Biol. Psychiatry 71:1 (2012), 15–21.
16. Copeland, W.E., Wolke, D., Lereya, S.T., Shanahan, L., Worthman, C.M., Costello, J.E., Childhood bullying involvement predicts low-grade systemic inflammation into adulthood. Proc. Natl. Acad. Sci. 111:21 (2014), 7570–7575.
17. Cuijpers, P., Vogelzangs, N., Twisk, J., Kleiboer, A., Li, J., Penninx, B.W., Comprehensive meta-analysis of excess mortality in depression in the general community versus patients with specific illnesses. Am. J. Psychiatry 171:4 (2014), 453–462.
18. Danese, A., Lewis, S.J., Psychoneuroimmunology of early-life stress: the hidden wounds of childhood trauma?. Neuropsychopharmacology 42 (2017), 99–114.
19. Danese, A., Pariante, C.M., Caspi, A., Taylor, A., Poulton, R., Childhood maltreatment predicts adult inflammation in a life-course study. Proc. Natl. Acad. Sci. 104:4 (2007), 1319–1324, 10.1073/pnas.0610362104.
20. Deverts, D.J., Cohen, S., DiLillo, V.G., Lewis, C.E., Kiefe, C., Whooley, M., Matthews, K.A., Depressive symptoms, race, and circulating C-reactive protein: the Coronary Artery Risk Development in Young Adults (CARDIA) study. Psychosom. Med. 72:8 (2010), 734–741.
21. Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E.K., Lanctôt, K.L., A meta-analysis of cytokines in major depression. Biol. Psychiatry 67:5 (2010), 446–457.
22. Evans, D.L., Charney, D.S., Lewis, L., Golden, R.N., Gorman, J.M., Krishnan, K.R.R., Coyne, J.C., Mood disorders in the medically ill: scientific review and recommendations. Biol. Psychiatry 58:3 (2005), 175–189.
23. Fagundes, C.P., Glaser, R., Hwang, B.S., Malarkey, W.B., Kiecolt-Glaser, J.K., Depressive symptoms enhance stress-induced inflammatory responses. Brain Behav. Immun. 31 (2013), 172–176.
24. Fagundes, C.P., Way, B.M., Early-life stress and adult inflammation. Curr. Directions Psychol. Sci. 23:4 (2014), 277–283.
25. Felitti, V.J., Anda, R.F., Nordenberg, D., Williamson, D.F., Spitz, A.M., Edwards, V., Marks, J.S., Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: The Adverse Childhood Experiences (ACE) Study. Am. J. Prev. Med. 14:4 (1998), 245–258.
26. Ferrante, A.W., Obesity-induced inflammation: a metabolic dialogue in the language of inflammation. J. Intern. Med. 262:4 (2007), 408–414.
27. Galcheva, S.V., Iotova, V.M., Yotov, Y.T., Bernasconi, S., Street, M.E., Circulating proinflammatory peptides related to adiposity and cardiometabolic risk factors in healthy prepubertal children. Eur. J. Endocrinol. 164 (2011), 553–558.
28. Garnett, S.P., Baur, L.A., Srinivasan, S.R., Lee, J.W., Cowell, C.T., Body mass index and waist circumference in midchildhood and adverse cardiovascular disease risk clustering in adolescence. Am. J. Clin. Nutr. 86:3 (2007), 549–555.
29. Gouin, J., Glaser, R., Malarkey, W.B., Beversdorf, D., Kiecolt-Glaser, J.K., Childhood abuse and inflammatory responses to daily stressors. Ann. Behav. Med. 44:2 (2012), 287–292.
30. Gunnar, M.R., Wewerka, S., Frenn, K., Long, J.D., Griggs, C., Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev. Psychopathol. 21:1 (2009), 69–85.
31. Haapakoski, R., Mathieu, J., Ebmeier, K.P., Alenius, H., Kivimäki, M., Cumulative meta-analysis of interleukins 6 and 1β tumour necrosis factor α and C-reactive protein in patients with major depressive disorder. Brain Behav. Immun. 49 (2015), 206–215.
32. Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: a regression-based approach: Guilford Press.
33. Hayes, A.F., An index and test of linear moderated mediation. Multivar. Behav. Res. 50:1 (2015), 1–22.
34. Hazel, N.A., Hammen, C., Brennan, P.A., Najman, J., Early childhood adversity and adolescent depression: the mediating role of continued stress. Psychol. Med. 38:04 (2008), 581–589.
35. Herder, C., Schneitler, S., Rathmann, W., Haastert, B., Schneitler, H., Winkler, H., Martin, S., Low-grade inflammation, obesity, and insulin resistance in adolescents. J. Clin. Endocrinol. Metabol. 92:12 (2007), 4569–4574.
36. Himmerich, H., Fulda, S., Linseisen, J., Seiler, H., Wolfram, G., Himmerich, S., Pollmächer, T., TNF-α soluble TNF receptor and interleukin-6 plasma levels in the general population. Eur. Cytokine Netw. 17:3 (2006), 196–201.
37. Howren, M.B., Lamkin, D.M., Suls, J., Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 71:2 (2009), 171–186.
38. Irwin, M.R., Cole, S.W., Reciprocal regulation of the neural and innate immune systems. Nat. Rev. Immunol. 11:9 (2011), 625–632, 10.1038/nri3042.
39. Janssen, I., Katzmarzyk, P.T., Srinivasan, S.R., Chen, W., Malina, R.M., Bouchard, C., Berenson, G.S., Combined influence of body mass index and waist circumference on coronary artery disease risk factors among children and adolescents. Pediatrics 115:6 (2005), 1623–1630.
40. Janusek, L.W., Tell, D., Gaylord-Harden, N., Mathews, H.L., Relationship of childhood adversity and neighborhood violence to a proinflammatory phenotype in emerging adult African American men: an epigenetic link. Brain Behav. Immun. 60 (2017), 126–135.
41. Katzmarzyk, P.T., Srinivasan, S.R., Chen, W., Malina, R.M., Bouchard, C., Berenson, G.S., Body mass index, waist circumference, and clustering of cardiovascular disease risk factors in a biracial sample of children and adolescents. Pediatrics 114:2 (2004), e198–e205.
42. Kessler, R.C., Avenevoli, S., Merikangas, K.R., Mood disorders in children and adolescents: an epidemiologic perspective. Biol. Psychiatry 49:12 (2001), 1002–1014.
43. Kidd, T., Carvalho, L.A., Steptoe, A., The relationship between cortisol responses to laboratory stress and cortisol profiles in daily life. Biol. Psychol. 99 (2014), 34–40.
44. Kirschbaum, C., Pirke, K.M., Hellhammer, D.H., The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:1–2 (1993), 76–81.
45. Kubzansky, L.D., Gilthorpe, M.S., Goodman, E., A prospective study of psychological distress and weight status in adolescents/young adults. Ann. Behav. Med. 43:2 (2012), 219–228.
46. Lacey, R.E., Kumari, M., Bartley, M., Social isolation in childhood and adult inflammation: evidence from the National Child Development Study. Psychoneuroendocrinology 50 (2014), 85–94.
47. Libby, P., Inflammation in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 32:9 (2012), 2045–2051.
48. Liu, Y., Ho, R.C., Mak, A., Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J. Affect. Disord. 139:3 (2012), 230–239.
49. MacMillan, H.L., Fleming, J.E., Streiner, D.L., Lin, E., Boyle, M.H., Jamieson, E., Beardslee, W.R., Childhood abuse and lifetime psychopathology in a community sample. Am. J. Psychiatry 158:11 (2001), 1878–1883.
50. Matthews, K.A., Chang, Y.F., Thurston, R.C., Bromberger, J.T., Child abuse is related to inflammation in mid-life women: Role of obesity. Brain Behav. Immun., 36(29–34), 2014.
51. Matthews, K.A., Schott, L.L., Bromberger, J.T., Cyranowski, J.M., Everson-Rose, S.A., Sowers, M.F., Are there bi-directional associations between depressive symptoms and C-reactive protein in mid-life women?. Brain Behav. Immun. 24:1 (2010), 96–101.
52. McEwen, B.S., Seeman, T., Protective and damaging effects of mediators of stress: elaborating and testing the concepts of allostasis and allostatic load. Ann. N. Y. Acad. Sci. 896:1 (1999), 30–47.
53. McInnis, C.M., Thoma, M.V., Gianferante, D., Hanlin, L., Chen, X., Breines, J.G., Rohleder, N., Measures of adiposity predict interleukin-6 responses to repeated psychosocial stress. Brain Behav. Immun. 42 (2014), 33–40.
54. McKeown, R.E., Garrison, C.Z., Jackson, K.L., Cuffe, S.P., Addy, C.L., Waller, J.L., Family structure and cohesion, and depressive symptoms in adolescents. J. Res. Adolesc. 7:3 (1997), 267–281.
55. McNelis, J.C., Olefsky, J.M., Macrophages, immunity, and metabolic disease. Immunity 41:1 (2014), 36–48.
56. Miller, G.E., Chen, E., Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychol. Sci. 21:6 (2010), 848–856.
57. Miller, G.E., Chen, E., Parker, K.J., Psychological stress in childhood and susceptibility to the chronic diseases of aging: moving toward a model of behavioral and biological mechanisms. Psychol. Bull. 137:6 (2011), 959–997, 10.1037/a0024768.
58. Miller, G.E., Cole, S.W., Clustering of depression and inflammation in adolescents previously exposed to childhood adversity. Biol. Psychiatry 72:1 (2012), 34–40.
59. Miller, G.E., Rohleder, N., Cole, S.W., Chronic interpersonal stress predicts activation of pro-and anti-inflammatory signaling pathways 6 months later. Psychosom. Med. 71:1 (2009), 57–62.
60. Norman, R.E., Byambaa, M., De, R., Butchart, A., Scott, J., Vos, T., The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLoS Med., 9(11), 2012, e1001349.
61. Nusslock, R., Miller, G.E., Early-life adversity and physical and emotional health across the lifespan: a neuroimmune network hypothesis. Biol. Psychiatry 80:1 (2016), 23–32.
62. O'Hara, R.E., Armeli, S., Boynton, M.H., Tennen, H., Emotional stress-reactivity and positive affect among college students: the role of depression history. Emotion, 14(1), 2014, 193.
63. Pace, T., Mletzko, T., Alagbe, O., Musselman, D., Nemeroff, C.B., Miller, A., Heim, C., Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry 163:9 (2006), 1630–1633.
64. Panagiotakos, D.B., Pitsavos, C., Yannakoulia, M., Chrysohoou, C., Stefanadis, C., The implication of obesity and central fat on markers of chronic inflammation: the ATTICA study. Atherosclerosis 183:2 (2005), 308–315.
65. Parent, J., Forehand, R., Dunbar, J.P., Watson, K.H., Reising, M.M., Seehuus, M., Compas, B.E., Parent and adolescent reports of parenting when a parent has a history of depression: associations with observations of parenting. J. Abnorm. Child Psychol. 42:2 (2014), 173–183.
66. Pietrobelli, A., Faith, M.S., Allison, D.B., Gallagher, D., Chiumello, G., Heymsfield, S.B., Body mass index as a measure of adiposity among children and adolescents: a validation study. J. Pediatr. 132:2 (1998), 204–210.
67. Pradhan, A.D., Manson, J.E., Rifai, N., Buring, J.E., Ridker, P.M., C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. J. Am. Med. Assoc. 286:3 (2001), 327–334.
68. Pruessner, J.C., Kirschbaum, C., Meinlschmid, G., Hellhammer, D.H., Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:7 (2003), 916–931.
69. Radloff, L.S., The CES-D scale: a self-report depression scale for research in the general population. Appl. Psychol. Meas. 1:3 (1977), 385–401.
70. Repetti, R.L., Robles, T.F., Reynolds, B., Allostatic processes in the family. Dev. Psychopathol. 22 (2011), 921–938.
71. Rodriguez, A.C.I., Epel, E.S., White, M.L., Standen, E.C., Seckl, J.R., Tomiyama, A.J., Hypothalamic-pituitary-adrenal axis dysregulation and cortisol activity in obesity: a systematic review. Psychoneuroendocrinology 62 (2015), 301–318.
72. Rohleder, N., Stimulation of systemic low-grade inflammation by psychosocial stress. Psychosom. Med. 76:3 (2014), 181–189.
73. Rotella, F., & Mannucci, E. (2013). Depression as a risk factor for diabetes: a meta-analysis of longitudinal studies. Journal of Clinical Psychiatry, 74, 31–37).
74. Schreier, H.M.C., Roy, L.B., Frimer, L.T., Chen, E., Family chaos and adolescent inflammatory profiles: The moderating role of socioeconomic status. Psychosom. Med. 76:6 (2014), 460–467.
75. Sebastian, C., Viding, E., Williams, K.D., Blakemore, S.J., Social brain development and the affective consequences of ostracism in adolescence. Brain Cogn. 72:1 (2010), 134–145.
76. Sheeber, L., Hops, H., Alpert, A., Davis, B., Andrews, J., Family support and conflict: prospective relations to adolescent depression. J. Abnorm. Child Psychol. 25:4 (1997), 333–344.
77. Slavich, G.M., Way, B.M., Eisenberger, N.I., Taylor, S.E., Neural sensitivity to social rejection is associated with inflammatory responses to social stress. Proc. Natl. Acad. Sci. 107:33 (2010), 14817–14822.
78. Slopen, N., Kubzansky, L.D., McLaughlin, K.A., Koenen, K.C., Childhood adversity and inflammatory processes in youth: a prospective study. Psychoneuroendocrinology 38:2 (2013), 188–200.
79. Somerville, L.H., The teenage brain: sensitivity to social evaluation. Curr. Directions Psychol. Sci. 22:2 (2013), 121–127.
80. Spear, L.P., Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 21:01 (2009), 87–97.
81. Spence, S.H., Najman, J.M., Bor, W., O'Callaghan, M.J., Williams, G.M., Maternal anxiety and depression, poverty and marital relationship factors during early childhood as predictors of anxiety and depressive symptoms in adolescence. J. Child Psychol. Psychiatry 43:4 (2002), 457–469.
82. St Clair, M.C., Croudace, T., Dunn, V.J., Jones, P.B., Herbert, J., Goodyer, I.M., Childhood adversity subtypes and depressive symptoms in early and late adolescence. Dev. Psychopathol. 27:03 (2015), 885–899.
83. Steene-Johannessen, J., Kolie, E., Reseland, J.E., Anderssen, S.A., Andersen, L.B., Waist circumference is related to low-grade inflammation in youth. Int. J. Pediatr. Obes. 5:4 (2010), 313–319.
84. Steptoe, A., Hamer, M., Chida, Y., The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 21:7 (2007), 901–912.
85. Strong, J.P., Malcom, G.T., McMahan, C.A., Tracy, R.E., Newman, W.P. III, Herderick, E.E., Cornhill, J.F., Prevalence and extent of atherosclerosis in adolescents and young adults: implications for prevention from the Pathobiological Determinants of Atherosclerosis in Youth Study. J. Am. Med. Assoc. 281:8 (1999), 727–735.
86. Stroud, L.R., Foster, E., Papandonatos, G.D., Handwerger, K., Granger, D.A., Kivlighan, K.T., Niaura, R., Stress response and the adolescent transition: performance versus peer rejection stressors. Dev. Psychopathol. 21:01 (2009), 47–68.
87. Taylor, R.W., Jones, I.E., Williams, S.M., Goulding, A., Evaluation of waist circumference, waist-to-hip ratio, and the conicity index as screening tools for high trunk fat mass, as measured by dual-energy X-ray absorptiometry, in children aged 3–19 y. Am. J. Clin. Nutr. 72:2 (2000), 490–495.
88. Taylor, S.E., Lehman, B.J., Kiefe, C.I., Seeman, T.E., Relationship of early life stress and psychological functioning to adult C-reactive protein in the Coronary Artery Risk Development in Young Adults Study. Biol. Psychiatry 60:8 (2006), 819–824.
89. Taylor, S.E., Lerner, J.S., Sage, R.M., Lehman, B.J., Seeman, T.E., Early environment, emotions, responses to stress, and health. J. Pers. 72:6 (2004), 1365–1394.
90. Weisberg, S.P., McCann, D.C., Desai, M., Rosenbaum, M., Leibel, R.L., Ferrante, A.W., Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Investig. 112:12 (2003), 1796–1808.
91. Wirtz, P.H., Ehlert, U., Emini, L., Suter, T., Higher body mass index (BMI) is associated with reduced glucocorticoid inhibition of inflammatory cytokine production following acute psychosocial stress in men. Psychoneuroendocrinology 33:8 (2008), 1102–1110.
92. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., La'Tonia, M.S., Bailey, M.T., Sheridan, J.F., Β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31:17 (2011), 6277–6288.
93. Xu, H., Barnes, G.T., Yang, Q., Tan, G., Yang, D., Chou, C.J., Tartaglia, L.A., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Investig. 112:12 (2003), 1821–1830.
94. Yudkin, J.S., Kumari, M., Humphries, S.E., Mohamed-Ali, V., Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link?. Atherosclerosis 148:2 (2000), 209–214.