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Reduced immunity to measles in adults with major depressive disorder

Published online by Cambridge University Press:  19 March 2018

Bart N. Ford*
Affiliation:
Laureate Institute for Brain Research, Tulsa, OK, USA The University of Tulsa Department of Biological Sciences, Tulsa, OK, USA
Robert H. Yolken
Affiliation:
Stanley Division of Developmental Neurovirology, Johns Hopkins University, Baltimore, MD, USA
Faith B. Dickerson
Affiliation:
Sheppard Pratt Health System, Baltimore, MD, USA
T. Kent Teague
Affiliation:
Departments of Surgery and Psychiatry, University of Oklahoma School of Community Medicine, Department of Biochemistry and Microbiology, Oklahoma State University Center for Health Sciences, Tulsa, OK, USA
Michael R. Irwin
Affiliation:
Cousins Center for Psychoneuroimmunology at UCLA, Semel Institute for Neuroscience and UCLA David Geffen School of Medicine, Los Angeles, CA, USA
Martin P. Paulus
Affiliation:
Laureate Institute for Brain Research, Tulsa, OK, USA
Jonathan Savitz
Affiliation:
Laureate Institute for Brain Research, Tulsa, OK, USA Oxley College of Health Sciences, The University of Tulsa, Tulsa, OK, USA
*
Author for correspondence: Bart Ford, E-mail: bford@laureateinstitute.org

Abstract

Background

Depression can impair the immunogenicity of vaccine administration in adults. Whereas many vaccinations are administered in childhood, it is not known whether adolescent or adult onset depression is associated with impairments in the maintenance of protection of childhood vaccines. This study tested the hypothesis that individuals with adolescent or adult onset mood disorders would display compromised immunity to measles, a target of childhood vaccination.

Methods

IgG antibodies to measles were quantified using a solid phase immunoassay in volunteers with bipolar disorder (BD, n = 64, mean age of onset = 16.6 ± 5.6), currently depressed individuals with major depressive disorder (cMDD, n = 85, mean age of onset = 17.9 ± 7.0), remitted individuals with a history of MDD (rMDD, n = 82, mean age of onset = 19.2 ± 8.6), and non-depressed comparison controls (HC, n = 202), all born after the introduction of the measles vaccine in the USA in 1963.

Results

Relative to HC, both the cMDD group (p = 0.021, adjusted odds ratios (OR) = 0.47, confidence interval (CI) = 0.24–0.90), and the rMDD group (p = 0.038, adjusted OR = 0.50, CI = 0.26–0.97) were less likely to test seropositive for measles. Compared with unmedicated MDD participants, currently medicated MDD participants had a longer lifetime duration of illness and were less likely to test seropositive for measles.

Conclusions

Individuals with adolescent or adult onset MDD are less likely to test seropositive for measles. Because lower IgG titers are associated with increased risk of measles infection, MDD may increase the risk and severity of infection possibly because of impaired maintenance of vaccine-related protection from measles.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

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References

Afsar, B, Elsurer, R, Eyileten, T, Yilmaz, MI and Caglar, K (2009) Antibody response following hepatitis B vaccination in dialysis patients: does depression and life quality matter? Vaccine 27, 58655869.Google Scholar
Besedovsky, HO, del Rey, A, Sorkin, E, Da Prada, M and Keller, HH (1979) Immunoregulation mediated by the sympathetic nervous system. Cellular Immunology 48, 346355.Google Scholar
Blume, J, Douglas, SD and Evans, DL (2011) Immune suppression and immune activation in depression. Brain, Behavior, and Immunity 25, 221229.Google Scholar
Bochennek, K, Allwinn, R, Langer, R, Becker, M, Keppler, OT, Klingebiel, T et al. (2014) Differential loss of humoral immunity against measles, mumps, rubella and varicella-zoster virus in children treated for cancer. Vaccine 32, 33573361.Google Scholar
Centers for Disease Control and Prevention (CDC) (2012) Measles - United States, 2011. MMWR. Morbidity and Mortality Weekly Report 61, 253257.Google Scholar
Chen, RT, Markowitz, LE, Albrecht, P, Stewart, JA, Mofenson, LM, Preblud, SR et al. (1990) Measles antibody: reevaluation of protective titers. The Journal of Infectious Diseases 162, 10361042.Google Scholar
Clemmons, NS, Gastanaduy, PA, Fiebelkorn, AP, Redd, SB and Wallace, GS, Centers for Disease Control and Prevention (CDC) (2015) Measles - United States, January 4-April 2, 2015. MMWR. Morbidity and Mortality Weekly Report 64, 373376.Google Scholar
Cohen, S and Williamson, GM (1991) Stress and infectious disease in humans. Psychological Bulletin 109, 524.Google Scholar
Davidkin, I, Jokinen, S, Broman, M, Leinikki, P and Peltola, H (2008) Persistence of measles, mumps, and rubella antibodies in an MMR-vaccinated cohort: a 20-year follow-up. The Journal of Infectious Diseases 197, 950956.Google Scholar
Dine, MS, Hutchins, SS, Thomas, A, Williams, I, Bellini, WJ and Redd, SC (2004) Persistence of vaccine-induced antibody to measles 26–33 years after vaccination. The Journal of Infectious Diseases 189(suppl. 1), S123S130.Google Scholar
Feenstra, B, Pasternak, B, Geller, F, Carstensen, L, Wang, T, Huang, F et al. (2014) Common variants associated with general and MMR vaccine-related febrile seizures. Nature Genetics 46, 12741282.Google Scholar
Fiebelkorn, AP, Redd, SB, Gallagher, K, Rota, PA, Rota, J, Bellini, W et al. (2010) Measles in the United States during the postelimination era. The Journal of Infectious Diseases 202, 15201528.Google Scholar
Glaser, R, Sheridan, J, Malarkey, WB, MacCallum, RC and Kiecolt-Glaser, JK (2000) Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine. Psychosomatic Medicine 62, 804807.Google Scholar
Gobin, V, Van Steendam, K, Denys, D and Deforce, D (2014) Selective serotonin reuptake inhibitors as a novel class of immunosuppressants. International Immunopharmacology 20, 148156.Google Scholar
Haralambieva, IH, Ovsyannikova, IG, Kennedy, RB, Larrabee, BR, Zimmermann, MT, Grill, DE et al. (2017) Genome-wide associations of CD46 and IFI44L genetic variants with neutralizing antibody response to measles vaccine. Human Genetics 136, 421435.Google Scholar
Haralambieva, IH, Ovsyannikova, IG, Pankratz, VS, Kennedy, RB, Jacobson, RM and Poland, GA (2013) The genetic basis for interindividual immune response variation to measles vaccine: new understanding and new vaccine approaches. Expert Review of Vaccines 12, 5770.Google Scholar
Holzmann, H, Hengel, H, Tenbusch, M and Doerr, HW (2016) Eradication of measles: remaining challenges. Medical Microbiology and Immunology 205, 201208.Google Scholar
Irwin, MR, Levin, MJ, Carrillo, C, Olmstead, R, Lucko, A, Lang, N et al. (2011) Major depressive disorder and immunity to varicella-zoster virus in the elderly. Brain, Behavior, and Immunity 25, 759766.Google Scholar
Irwin, MR, Levin, MJ, Laudenslager, ML, Olmstead, R, Lucko, A, Lang, N et al. (2013) Varicella zoster virus-specific immune responses to a herpes zoster vaccine in elderly recipients with major depression and the impact of antidepressant medications. Clinical Infectious Diseases: an Official Publication of the Infectious Diseases Society of America 56, 10851093.Google Scholar
Kano, H, Mizuta, K, Sakakihara, Y, Kato, H, Miki, Y, Shibuya, N et al. (2002) Efficacy and safety of immunization for pre- and post- liver transplant children. Transplantation 74, 543550.Google Scholar
Kassebaum, NJ, Smith, AGC, Bernabé, E, Fleming, TD, Reynolds, AE, Vos, T et al. GBD 2015 Oral Health Collaborators (2017) Global, Regional, and National prevalence, incidence, and disability-adjusted life years for oral conditions for 195 countries, 1990–2015: a systematic analysis for the global burden of diseases, injuries, and risk factors. Journal of Dental Research 96, 380387.Google Scholar
Kennedy, RB, Ovsyannikova, IG, Haralambieva, IH, O'Byrne, MM, Jacobson, RM, Pankratz, VS et al. (2012) Multigenic control of measles vaccine immunity mediated by polymorphisms in measles receptor, innate pathway, and cytokine genes. Vaccine 30, 21592167.Google Scholar
Kessler, RC, Petukhova, M, Sampson, NA, Zaslavsky, AM and Wittchen, H-U (2012) Twelve-month and lifetime prevalence and lifetime morbid risk of anxiety and mood disorders in the United States. International Journal of Methods in Psychiatric Research 21, 169184.Google Scholar
Kiecolt-Glaser, JK, Glaser, R, Gravenstein, S, Malarkey, WB and Sheridan, J (1996) Chronic stress alters the immune response to influenza virus vaccine in older adults. Proceedings of the National Academy of Sciences of the United States of America 93, 30433047.Google Scholar
McLean, HQ, Fiebelkorn, AP, Temte, JL and Wallace, GS, Centers for Disease Control and Prevention (2013) Prevention of measles, rubella, congenital rubella syndrome, and mumps, 2013: summary recommendations of the advisory committee on immunization practices (ACIP). MMWR. Recommendations and Reports: Morbidity and Mortality Weekly Report. Recommendations and Reports/Centers for Disease Control 62, 134.Google Scholar
Measles Cases and Outbreaks (2017) Center for Disease Control and Prevention.Google Scholar
Measles Fact Sheet (2017) World Health Organization.Google Scholar
Miller, GE, Cohen, S, Pressman, S, Barkin, A, Rabin, BS and Treanor, JJ (2004) Psychological stress and antibody response to influenza vaccination: when is the critical period for stress, and how does it get inside the body? Psychosomatic Medicine 66, 215223.Google Scholar
Mossong, J, Nokes, DJ, Edmunds, WJ, Cox, MJ, Ratnam, S and Muller, CP (1999) Modeling the impact of subclinical measles transmission in vaccinated populations with waning immunity. American Journal of Epidemiology 150, 12381249.Google Scholar
Prather, AA, Hall, M, Fury, JM, Ross, DC, Muldoon, MF, Cohen, S et al. (2012) Sleep and antibody response to hepatitis B vaccination. Sleep 35, 10631069.Google Scholar
Redd, SC, King, GE, Heath, JL, Forghani, B, Bellini, WJ and Markowitz, LE (2004) Comparison of vaccination with measles-mumps-rubella vaccine at 9, 12, and 15 months of age. The Journal of Infectious Diseases 189(suppl. 1), S116S122.Google Scholar
Rocca, S, Santilli, V, Cotugno, N, Concato, C, Manno, EC, Nocentini, G et al. (2016) Waning of vaccine-induced immunity to measles in kidney transplanted children. Medicine 95, e4738.Google Scholar
Ruderfer, DM, Fanous, AH, Ripke, S, McQuillin, A, Amdur, RL, Schizophrenia Working Group of Psychiatric Genomics Consortium, Bipolar Disorder Working Group of Psychiatric Genomics Consortium, Cross-Disorder Working Group of Psychiatric Genomics Consortium, Gejman, PV et al. (2014) Polygenic dissection of diagnosis and clinical dimensions of bipolar disorder and schizophrenia. Molecular Psychiatry 19, 10171024.Google Scholar
Sanders, VM (2006) Interdisciplinary research: noradrenergic regulation of adaptive immunity. Brain, Behavior, and Immunity 20, 18.Google Scholar
Segerstrom, SC, Hardy, JK, Evans, DR and Greenberg, RN (2012) Vulnerability, distress, and immune response to vaccination in older adults. Brain, Behavior, and Immunity 26, 747753.Google Scholar
Seither, R, Calhoun, K, Mellerson, J, Knighton, CL, Street, E, Dietz, V et al. (2016) Vaccination coverage among children in kindergarten - United States, 2015–16 school year. MMWR. Morbidity and Mortality Weekly Report 65, 10571064.Google Scholar
Spiegel, K, Sheridan, JF and Van Cauter, E (2002) Effect of sleep deprivation on response to immunization. JAMA: the Journal of the American Medical Association 288, 14711472.Google Scholar
Suzuki, H, Savitz, J, Kent Teague, T, Gandhapudi, SK, Tan, C, Misaki, M et al. (2017) Altered populations of natural killer cells, cytotoxic T lymphocytes, and regulatory T cells in major depressive disorder: association with sleep disturbance. Brain, Behavior, and Immunity 66, 193200.Google Scholar
Titanji, K, De Milito, A, Cagigi, A, Thorstensson, R, Grützmeier, S, Atlas, A et al. (2006) Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 108, 15801587.Google Scholar
Vedhara, K, Cox, NK, Wilcock, GK, Perks, P, Hunt, M, Anderson, S et al. (1999) Chronic stress in elderly carers of dementia patients and antibody response to influenza vaccination. The Lancet 353, 627631.Google Scholar
Warmington, L, Lee, BE and Robinson, JL (2005) Loss of antibodies to measles and varicella following solid organ transplantation in children. Pediatric Transplantation 9, 311314.Google Scholar
Zhang, C, Wu, Z, Zhao, G, Wang, F and Fang, Y (2016) Identification of IL6 as a susceptibility gene for major depressive disorder. Scientific Reports 6, 31264.Google Scholar
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