Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2025-01-03T14:35:46.049Z Has data issue: false hasContentIssue false
  • English
  • Français

Depressive symptoms and immune response to meningococcal conjugate vaccine in early adolescence

Published online by Cambridge University Press:  25 November 2014

Thomas G. O'Connor ,
Jan A. Moynihan ,
Peter A. Wyman ,
Jennifer Carnahan ,
Gerry Lofthus ,
Sally A. Quataert ,
Melissa Bowman  and
Mary T. Caserta
Thomas G. O'Connor*
Affiliation:
Wynne Center for Family Research University of Rochester Medical Center
Jan A. Moynihan
Affiliation:
University of Rochester Medical Center
Peter A. Wyman
Affiliation:
University of Rochester Medical Center
Jennifer Carnahan
Affiliation:
University of Rochester Medical Center
Gerry Lofthus
Affiliation:
University of Rochester Medical Center
Sally A. Quataert
Affiliation:
University of Rochester Medical Center
Melissa Bowman
Affiliation:
University of Rochester Medical Center
Mary T. Caserta*
Affiliation:
University of Rochester Medical Center
*
Address correspondence and reprint requests to: Thomas G. O'Connor, Department of Psychiatry, Wynne Center for Family Research, University of Rochester Medical Center, 300 Crittenden Blvd, Rochester, NY 14642; E-mail: [email protected]; or Mary T. Caserta, Department of Pediatrics, University of Rochester Medical Center, 601 Elmwood Avenue, Rochester, NY 14642; E-mail: [email protected].
Address correspondence and reprint requests to: Thomas G. O'Connor, Department of Psychiatry, Wynne Center for Family Research, University of Rochester Medical Center, 300 Crittenden Blvd, Rochester, NY 14642; E-mail: [email protected]; or Mary T. Caserta, Department of Pediatrics, University of Rochester Medical Center, 601 Elmwood Avenue, Rochester, NY 14642; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Research findings in psychoneuroimmunology document reliable, bidirectional linkages among psychological processes, the nervous system, and the immune system. However, available data are based almost entirely on animal and adult human studies; the application to children and adolescents is uncertain. We capitalized on the experimental leverage provided by a routine vaccination to examine the link between mood symptoms and the immune response to a vaccine challenge in early adolescence. One hundred twenty-six 11-year-olds for whom vaccine response data were available were assessed at prevaccination and 4 weeks, 3 months, and 6 months following vaccination; self-report ratings of depression and anxiety as well as measures of psychosocial and somatic risk were assessed prior to vaccine response. Analyses indicated that children's internalizing mood symptoms were associated with elevated and persistently higher antibody responses, with evidence extending to two of the four serogroups. The associations remained after controlling for multiple possible confounders (social class, body mass index, sleep, psychosocial risk, and pubertal status). The observed enhanced vaccine response associated with depressive and anxious symptoms in early adolescence may reflect an important developmental difference in immune system–brain interplay between adults and children, and it underscores the need for further developmental studies of psychoneuroimmunology.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Special Issue 4pt2: Multilevel Developmental Perspectives Toward Understanding Internalizing Psychopathology: Current Research and Future Directions , November 2014 , pp. 1567 - 1576
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ader, R. (1983). Developmental psychoneuroimmunology. Developmental Psychobiology, 16, 251–267.CrossRefGoogle ScholarPubMed
Ader, R., & Cohen, N. (1975). Behaviorally conditioned immunosuppression. Psychosomatic Medicine, 37, 333–340.CrossRefGoogle ScholarPubMed
Ader, R., & Cohen, N. (1993). Psychoneuroimmunology: Conditioning and stress. Annual Review of Psychology, 44, 53–85.CrossRefGoogle ScholarPubMed
Ader, R., Cohen, N., & Felten, D. (1995). Psychoneuroimmunology: Interactions between the nervous system and the immune system. Lancet, 345, 99–103.CrossRefGoogle ScholarPubMed
Adler, N. E. (2000). The MacArthur Scale of Subjective Social Status. Retrieved from http://www.macses.ucsf.edu/Research/Psychosocial/notebook/subjective.html Google Scholar
Allgaier, A. K., Fruhe, B., Pietsch, K., Saravo, B., Baethmann, M., & Schulte-Korne, G. (2012). Is the Children's Depression Inventory short version a valid screening tool in pediatric care? A comparison to its full-length version. Journal of Psychosomatic Research, 73, 369–374.CrossRefGoogle ScholarPubMed
Angold, A., Weissman, M. M., John, K., Merikangas, K. R., Prusoff, B. A., Wickramaratne, P., et al. (1987). Parent and child reports of depressive symptoms in children at low and high risk of depression. Journal of Child Psychology and Psychiatry and Allied Disciplines, 28, 901–915.CrossRefGoogle ScholarPubMed
Ashwood, P., Krakowiak, P., Hertz-Picciotto, I., Hansen, R., Pessah, I. N., & Van de Water, J. (2011). Altered T cell responses in children with autism. Brain, Behavior, and Immunity, 25, 840–849.CrossRefGoogle ScholarPubMed
Avitsur, R., Stark, J. L., & Sheridan, J. F. (2001). Social stress induces glucocorticoid resistance in subordinate animals. Hormones and Behavior, 39, 247–257.CrossRefGoogle ScholarPubMed
Banks, W. A., Kastin, A. J., & Broadwell, R. D. (1995). Passage of cytokines across the blood–brain barrier. Neuroimmunomodulation, 2, 241–248.CrossRefGoogle ScholarPubMed
Bauer, M. E. (2008). Chronic stress and immunosenescence: A review. Neuroimmunomodulation, 15, 241–250.CrossRefGoogle ScholarPubMed
Blackmore, E. R., Moynihan, J. A., Rubinow, D. R., Pressman, E. K., Gilchrist, M., & O'Connor, T. G. (2011). Psychiatric symptoms and proinflammatory cytokines in pregnancy. Psychosomatic Medicine, 73, 656–663.CrossRefGoogle ScholarPubMed
Borrow, R., Goldblatt, D., Finn, A., Southern, J., Ashton, L., Andrews, N., et al. (2003). Immunogenicity of, and immunologic memory to, a reduced primary schedule of meningococcal C-tetanus toxoid conjugate vaccine in infants in the United kingdom. Infection and Immunity, 71, 5549–5555.CrossRefGoogle ScholarPubMed
Burns, V. E., Drayson, M., Ring, C., & Carroll, D. (2002). Perceived stress and psychological well-being are associated with antibody status after meningitis C conjugate vaccination. Psychosomatic Medicine, 64, 963–970.Google ScholarPubMed
Caserta, M. T., O'Connor, T. G., Wyman, P. A., Wang, H., Moynihan, J., Cross, W., et al. (2008). The associations between psychosocial stress and the frequency of illness, and innate and adaptive immune function in children. Brain, Behavior, and Immunity, 2, 933–940.CrossRefGoogle Scholar
Caserta, M. T., Wyman, P. A., Wang, H., Moynihan, J., & O'Connor, T. G. (2011). Associations among depression, perceived self-efficacy, and immune function and health in preadolescent children. Development and Psychopathology, 23, 1139–1147.CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention. (2005). Prevention and Control of Meningococcal Disease Recommendations of the Advisory Committee on Immunization Practices (ACIP). Morbidity and Mortality Weekly Report, 54, 1–21.Google Scholar
Coe, C. L. (1996). Developmental psychoneuroimmunology revisited. Brain, Behavior, and Immunity, 10, 185–187.CrossRefGoogle ScholarPubMed
Cowen, E. L., Work, W. C., Hightower, A. D., Wyman, P. A., Parker, G. R., & Lotyczewski, B. S. (1991). Toward the development of a measure of perceived self-efficacy in children. Journal of Clinical Child Psychology, 20, 169–178.CrossRefGoogle Scholar
Creswell, J. D., Irwin, M. R., Burklund, L. J., Lieberman, M. D., Arevalo, J. M., Ma, J., et al. (2012). Mindfulness-based stress reduction training reduces loneliness and pro-inflammatory gene expression in older adults: A small randomized controlled trial. Brain, Behavior, and Immunity, 26, 1095–1101.CrossRefGoogle ScholarPubMed
Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., & Kelley, K. W. (2008). From inflammation to sickness and depression: When the immune system subjugates the brain. Nature Reviews Neuroscience, 9, 46–56.CrossRefGoogle ScholarPubMed
Derogatis, L. R. (1992). BSI: Administration, scoring, and procedures manual—II. Baltimore, MD: Clinical Psychometric Research.Google Scholar
Derogatis, L. R., & Melisaratos, N. (1983). The Brief Symptom Inventory: An introductory report. Psychological Medicine, 13, 595–605.CrossRefGoogle ScholarPubMed
Dhabhar, F. S. (2009). Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation, 16, 300–317.CrossRefGoogle ScholarPubMed
Edwards, K. M., Burns, V. E., Adkins, A. E., Carroll, D., Drayson, M., & Ring, C. (2008). Meningococcal A vaccination response is enhanced by acute stress in men. Psychosomatic Medicine, 70, 147–151.CrossRefGoogle ScholarPubMed
Edwards, K. M., Burns, V. E., Reynolds, T., Carroll, D., Drayson, M., & Ring, C. (2006). Acute stress exposure prior to influenza vaccination enhances antibody response in women. Brain, Behavior, and Immunity, 20, 159–168.CrossRefGoogle ScholarPubMed
Edwards, K. M., Pung, M. A., Tomfohr, L. M., Ziegler, M. G., Campbell, J. P., Drayson, M. T., et al. (2012). Acute exercise enhancement of pneumococcal vaccination response: A randomised controlled trial of weaker and stronger immune response. Vaccine, 30, 6389–6395.CrossRefGoogle ScholarPubMed
Franceschi, C., Bonafe, M., Valensin, S., Olivieri, F., De Luca, M., Ottaviani, E., et al. (2000). Inflamm-aging: An evolutionary perspective on immunosenescence. Annals of the New York Academy of Sciences, 908, 244–254.CrossRefGoogle ScholarPubMed
Gallagher, S., Phillips, A. C., Drayson, M. T., & Carroll, D. (2009). Caregiving for children with developmental disabilities is associated with a poor antibody response to influenza vaccination. Psychosomatic Medicine, 71, 341–344.CrossRefGoogle ScholarPubMed
Gheesling, L. L., Carlone, G. M., Pais, L. B., Holder, P. F., Maslanka, S. E., Plikaytis, B. D., et al. (1994). Multicenter comparison of Neisseria meningitidis serogroup C anti-capsular polysaccharide antibody levels measured by a standardized enzyme-linked immunosorbent assay. Journal of Clinical Microbiology, 32, 1475–1482.CrossRefGoogle ScholarPubMed
Glaser, R., Sheridan, J., Malarkey, W. B., MacCallum, R. C., & Kiecolt-Glaser, J. K. (2000). Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine. Psychosomatic Medicine, 62, 804–807.CrossRefGoogle ScholarPubMed
Goodman, E., Adler, N. E., Kawachi, I., Frazier, A. L., Huang, B., & Colditz, G. A. (2001). Adolescents' perceptions of social status: Development and evaluation of a new indicator. Pediatrics, 108, E31.CrossRefGoogle ScholarPubMed
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.CrossRefGoogle ScholarPubMed
Henje Blom, E., Lekander, M., Ingvar, M., Asberg, M., Mobarrez, F., & Serlachius, E. (2012). Pro-inflammatory cytokines are elevated in adolescent females with emotional disorders not treated with SSRIs. Journal of Affective Disorders, 136, 716–723.CrossRefGoogle Scholar
Irwin, M., Patterson, T., Smith, T. L., Caldwell, C., Brown, S. A., Gillin, J. C., et al. (1990). Reduction of immune function in life stress and depression. Biological Psychiatry, 27, 22–30.CrossRefGoogle ScholarPubMed
Kelley, K. W., Arkins, S., & Li, Y. M. (1992). Growth hormone, prolactin, and insulin-like growth factors: New jobs for old players. Brain, Behavior, and Immunity, 6, 317–326.CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, J. K., Garner, W., Speicher, C., Penn, G. M., Holliday, J., & Glaser, R. (1984). Psychosocial modifiers of immunocompetence in medical students. Psychosomatic Medicine, 46, 7–14.CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, J. K., Glaser, R., Gravenstein, S., Malarkey, W. B., & Sheridan, J. (1996). Chronic stress alters the immune response to influenza virus vaccine in older adults. Proceedings of the National Academy of Sciences, 93, 3043–3047.CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, J. K., Loving, T. J., Stowell, J. R., Malarkey, W. B., Lemeshow, S., Dickinson, S. L., et al. (2005). Hostile marital interactions, proinflammatory cytokine production, and wound healing. Archives of General Psychiatry, 62, 1377–1384.CrossRefGoogle ScholarPubMed
Kollmann, T. R., Levy, O., Montgomery, R. R., & Goriely, S. (2012). Innate immune function by Toll-like receptors: Distinct responses in newborns and the elderly. Immunity, 37, 771–783.CrossRefGoogle ScholarPubMed
Kovacs, M. (2001). Manual for the Children's Depression Inventory. North Tonawanda, NY: Multi-Health Systems.Google Scholar
Kovacs, M. (2003). Children's Depression Inventory (CDI): Technical manual update. Toronto: Multi-Health Systems.Google Scholar
Meyer, R. J., & Haggerty, R. J. (1962). Streptococcal infections in families: Factors altering individual susceptibility. Pediatrics, 29, 539–549.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Miller, G. E., Kemeny, M. E., Taylor, S. E., Cole, S. W., & Visscher, B. R. (1997). Social relationships and immune processes in HIV seropositive gay and bisexual men. Annuals of Behavioral Medicine, 19, 139–151.CrossRefGoogle ScholarPubMed
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, 54, 816–835.CrossRefGoogle ScholarPubMed
Moynihan, J. A., Ader, R., Grota, L. J., Schachtman, T. R., & Cohen, N. (1990). The effects of stress on the development of immunological memory following low-dose antigen priming in mice. Brain, Behavior, and Immunity, 4, 1–12.CrossRefGoogle ScholarPubMed
Moynihan, J. A., Larson, M. R., Treanor, J., Duberstein, P. R., Power, A., Shore, B., et al. (2004). Psychosocial factors and the response to influenza vaccination in older adults. Psychosomatic Medicine, 66, 950–953.CrossRefGoogle ScholarPubMed
Muris, P., Merckelbach, H., Ollendick, T., King, N., & Bogie, N. (2002). Three traditional and three new childhood anxiety questionnaires: Their reliability and validity in a normal adolescent sample. Behaviour Research and Therapy, 40, 753–772.CrossRefGoogle Scholar
O'Connor, M. F., Bower, J. E., Cho, H. J., Creswell, J. D., Dimitrov, S., Hamby, M. E., et al. (2009). To assess, to control, to exclude: Effects of biobehavioral factors on circulating inflammatory markers. Brain, Behavior, and Immunity, 23, 887–897.CrossRefGoogle ScholarPubMed
O'Connor, T. G., Moynihan, J. A., & Caserta, M. T. (2014). Annual research review: The neuroinflammation hypothesis for stress and psychopathology in children—Developmental psychoneuroimmunology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 55, 615–631.CrossRefGoogle ScholarPubMed
O'Connor, T. G., Winter, M. A., Hunn, J., Carnahan, J., Pressman, E. K., Glover, V., et al. (2013). Prenatal maternal anxiety predicts reduced adaptive immunity in infants. Brain, Behavior, and Immunity, 32, 21–28.CrossRefGoogle ScholarPubMed
Powell, N. D., Allen, R. G., Hufnagle, A. R., Sheridan, J. F., & Bailey, M. T. (2011). Stressor-induced alterations of adaptive immunity to vaccination and viral pathogens. Immunology and Allergy Clinics of North America, 31, 69–79.CrossRefGoogle ScholarPubMed
PrabhuDas, M., Adkins, B., Gans, H., King, C., Levy, O., Ramilo, O., et al. (2011). Challenges in infant immunity: Implications for responses to infection and vaccines. Nature Immunology, 12, 189–194.CrossRefGoogle ScholarPubMed
Raison, C. L., Rutherford, R. E., Woolwine, B. J., Shuo, C., Schettler, P., Drake, D. F., et al. (2013). A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: The role of baseline inflammatory biomarkers. JAMA Psychiatry, 70, 31–41.CrossRefGoogle ScholarPubMed
Rennels, M., King, J. Jr., Ryall, R., Papa, T., & Froeschle, J. (2004). Dosage escalation, safety and immunogenicity study of four dosages of a tetravalent meninogococcal polysaccharide diphtheria toxoid conjugate vaccine in infants. Pediatric Infectious Disease Journal, 23, 429–435.CrossRefGoogle ScholarPubMed
Reynolds, C. R., & Richmond, B. O. (1985). Factor structure and construct validity of “What I think and feel”: The Revised Children's Manifest Anxiety Scale. Journal of Personality Assessment, 43, 281–283.CrossRefGoogle Scholar
Reynolds, C. R., & Richmond, B. O. (1997). What I think and feel: A revised measure of children's manifest anxiety. Journal of Abnormal Child Psychology, 25, 15–20.CrossRefGoogle Scholar
Schleifer, S. J., Bartlett, J. A., Keller, S. E., Eckholdt, H. M., Shiflett, S. C., & Delaney, B. R. (2002). Immunity in adolescents with major depression. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 1054–1060.CrossRefGoogle ScholarPubMed
Segerstrom, S. C., Hardy, J. K., Evans, D. R., & Greenberg, R. N. (2012). Vulnerability, distress, and immune response to vaccination in older adults. Brain, Behavior, and Immunity, 26, 747–753.CrossRefGoogle ScholarPubMed
Sheridan, J. F., Stark, J. L., Avitsur, R., & Padgett, D. A. (2000). Social disruption, immunity, and susceptibility to viral infection: Role of glucocorticoid insensitivity and NGF. Annuals of the New York Academy of Sciences, 917, 894–905.CrossRefGoogle ScholarPubMed
Sikkema, D. J., Friedman, K. E., Corsaro, B., Kimura, A., Hildreth, S. W., Madore, D. V., et al. (2000). Relationship between serum bactericidal activity and serogroup-specific immunoglobulin G concentration for adults, toddlers, and infants immunized with Neisseria meningitidis serogroup C vaccines. Clinical and Diagnostic Laboratory Immunology, 7, 764–768.CrossRefGoogle ScholarPubMed
Snyder, B. K., Roghmann, K. J., & Sigal, L. H. (1993). Stress and psychosocial factors: Effects on primary cellular immune response. Journal of Behavioral Medicine, 16, 143–161.CrossRefGoogle ScholarPubMed
Swedo, S. E., Garvey, M., Snider, L., Hamilton, C., & Leonard, H. L. (2001). The PANDAS subgroup: Recognition and treatment. CNS Spectrums, 6, 419–422, 425–426.CrossRefGoogle ScholarPubMed
Swedo, S. E., & Grant, P. J. (2005). Annotation: PANDAS: A model for human autoimmune disease. Journal of Child Psychology and Psychiatry and Allied Disciplines, 46, 227–234.CrossRefGoogle Scholar
Van Damme, P., Moiseeva, A., Marichev, I., Kervyn, A. D., Booy, R., Kuriyakose, S., et al. (2010). Five years follow-up following two or three doses of a hepatitis B vaccine in adolescents aged 11–15 years: A randomised controlled study. BMC Infectious Diseases, 10, 357.CrossRefGoogle ScholarPubMed
Vedhara, K., Cox, N. K., Wilcock, G. K., Perks, P., Hunt, M., Anderson, S., et al. (1999). Chronic stress in elderly carers of dementia patients and antibody response to influenza vaccination. Lancet, 353, 627–631.CrossRefGoogle ScholarPubMed
Weissman, M. M., Wickramaratne, P., Warner, V., John, K., Prusoff, B. A., Merikangas, K. R., et al. (1987). Assessing psychiatric disorders in children: Discrepancies between mothers’ and children's reports. Archives of General Psychiatry, 44, 747–753.CrossRefGoogle ScholarPubMed
Werner, H., Molinari, L., Guyer, C., & Jenni, O. G. (2008). Agreement rates between actigraphy, diary, and questionnaire for children's sleep patterns. Archives of Pediatrics and Adolescent Medicine, 162, 350–358.CrossRefGoogle ScholarPubMed
Wright, C. E., Strike, P. C., Brydon, L., & Steptoe, A. (2005). Acute inflammation and negative mood: Mediation by cytokine activation. Brain, Behavior, and Immunity, 19, 345–350.CrossRefGoogle ScholarPubMed
Wu, J. S., Hwang, L. Y., Goodman, K. J., & Beasley, R. P. (1999). Hepatitis B vaccination in high-risk infants: 10-year follow-up. Journal of Infectious Diseases, 179, 1319–1325.CrossRefGoogle Scholar
Wyman, P. A., Cowen, E. L., Work, W. C., Hoyt-Meyers, L., Magnus, K. B., & Fagen, D. B. (1999). Caregiving and developmental factors differentiating young at-risk urban children showing resilient versus stress-affected outcomes: A replication and extension. Child Development, 70, 645–659.CrossRefGoogle ScholarPubMed
Wyman, P. A., Cowen, E. L., Work, W. C., Kerley, J. H. (1993). The role of children's future expectations in self-system functioning and adjustment to life stress. Development and Psychopathology, 5, 649–661.CrossRefGoogle Scholar
Zanetti, A., Parlato, A., Romano, L., Desole, M. G., Ferrera, G., Giurdanella, F., et al. (2012). Challenge with a hepatitis B vaccine in two cohorts of 4-7-year-old children primed with hexavalent vaccines: An open-label, randomised trial in Italy. Vaccine, 30, 5770–5775.CrossRefGoogle ScholarPubMed