Association of Cytomegalovirus and Toxoplasma gondii Antibody Titers with Bipolar Disorder

JAMA Psychiatry

Volumn 76, Issue 12, 2019, Pages 1285-1293

  Frye, Mark A ^a   Coombes, Brandon J ^a   McElroy, Susan L ^b   Jones Brando, Lori ^c   Bond, David J ^d   Veldic, Marin ^a   Romo Nava, Francisco ^b   Bobo, William V ^e   Singh, Balwinder ^a   Colby, Colin ^a   Skime, Michelle K ^a   Biernacka, Joanna M ^a   Yolken, Robert ^c  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPROTOZOAL AGENT; C REACTIVE PROTEIN; CYTOMEGALOVIRUS ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MEASLES ANTIBODY; PROTOZOON ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; VIRUS ANTIBODY;

ADULT; ANTIBODY TITER; ARTICLE; BIOBANK; BIPOLAR DISORDER; BIPOLAR I DISORDER; BIPOLAR II DISORDER; BLOOD SAMPLING; CASE CONTROL STUDY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MANIC PSYCHOSIS; MEASLES; MEDICAL HISTORY; MINNESOTA; NONHUMAN; OHIO; ONSET AGE; PREVALENCE; SEROLOGY; TOXOPLASMOSIS; BLOOD; CLASSIFICATION; CYTOMEGALOVIRUS; IMMUNOLOGY; MIDDLE AGED; PATHOPHYSIOLOGY; TOXOPLASMA;

ADULT; ANTIBODIES, PROTOZOAN; ANTIBODIES, VIRAL; BIOLOGICAL SPECIMEN BANKS; BIPOLAR DISORDER; CASE-CONTROL STUDIES; CYTOMEGALOVIRUS; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MALE; MIDDLE AGED; TOXOPLASMA;

EID: 85072372282     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2019.2499     Document Type: Article

References (43)

1. Lazarus RS. From psychological stress to the emotions: a history of changing outlooks. Annu Rev Psychol. 1993; 44 (1): 1-21. doi: 10.1146/annurev.ps.44.020193.000245 8434890
2. Leboyer M, Berk M, Yolken RH, Tamouza R, Kupfer D, Groc L. Immuno-psychiatry: an agenda for clinical practice and innovative research. BMC Med. 2016; 14 (1): 173. doi: 10.1186/s12916-016-0712-5 27788673
3. Weissman MM, Bland RC, Canino GJ, Cross-national epidemiology of major depression and bipolar disorder. JAMA. 1996; 276 (4): 293-299. doi: 10.1001/jama.1996.03540040037030 8656541
4. Tedla Y, Shibre T, Ali O, Serum antibodies to Toxoplasma gondii and herpesvidae family viruses in individuals with schizophrenia and bipolar disorder: a case-control study. Ethiop Med J. 2011; 49 (3): 211-220. 21991754
5. Hamdani N, Daban-Huard C, Godin O, Effects of cumulative herpesviridae and Toxoplasma gondii infections on cognitive function in healthy, bipolar, and schizophrenia subjects. J Clin Psychiatry. 2017; 78 (1): e18-e27. doi: 10.4088/JCP.15m10133 27929612
6. Stich O, Andres TA, Gross CM, Gerber SI, Rauer S, Langosch JM. An observational study of inflammation in the central nervous system in patients with bipolar disorder. Bipolar Disord. 2015; 17 (3): 291-302. doi: 10.1111/bdi.12244 25109751
7. Rizzo LB, Do Prado CH, Grassi-Oliveira R, Immunosenescence is associated with human cytomegalovirus and shortened telomeres in type I bipolar disorder. Bipolar Disord. 2013; 15 (8): 832-838. doi: 10.1111/bdi.12121 24021055
8. Houenou J, d'Albis M-A, Daban C, Cytomegalovirus seropositivity and serointensity are associated with hippocampal volume and verbal memory in schizophrenia and bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2014; 48: 142-148. doi: 10.1016/j.pnpbp.2013.09.003 24083998
9. Prossin AR, Yolken RH, Kamali M, Cytomegalovirus antibody elevation in bipolar disorder: relation to elevated mood states. Neural Plast. 2015; 2015:
10. Simanek AM, Parry A, Dowd JB. Differences in the association between persistent pathogens and mood disorders among young-to middle-aged women and men in the US. Brain Behav Immun. 2018; 68: 56-65. doi: 10.1016/j.bbi.2017.09.017 28965957
11. Afifi MA, Jiman-Fatani AA, Al-Rabia MW, Al-Hussainy NH, El Saadany S, Mayah W. More than an association: latent Toxoplasmosis might provoke a local oxidative stress that triggers the development of bipolar disorder. J Microsc Ultrastruct. 2018; 6 (3): 139-144. doi: 10.4103/JMAU.JMAU-22-18 30221140
12. Burgdorf KS, Trabjerg BB, Pedersen MG, Large-scale study of toxoplasma and cytomegalovirus shows an association between infection and serious psychiatric disorders. Brain Behav Immun. 2019; 79 (January): 152-158. doi: 10.1016/j.bbi.2019.01.026 30685531
13. Leboyer M, Soreca I, Scott J, Can bipolar disorder be viewed as a multi-system inflammatory disease? J Affect Disord. 2012; 141 (1): 1-10. doi: 10.1016/j.jad.2011.12.049 22497876
14. Frye MA, McElroy SL, Fuentes M, Development of a bipolar disorder biobank: differential phenotyping for subsequent biomarker analyses. Int J Bipolar Disord. 2015; 3 (1): 30. doi: 10.1186/s40345-015-0030-4 26105627
15. Olson JE, Ryu E, Johnson KJ, The Mayo Clinic Biobank: a building block for individualized medicine. Mayo Clin Proc. 2013; 88 (9): 952-962. doi: 10.1016/j.mayocp.2013.06.006 24001487
16. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed, text revision. Washington, DC: American Psychiatric Association; 2000.
17. Akinhanmi MO, Biernacka JM, Strakowski SM, Racial disparities in bipolar disorder treatment and research: a call to action. Bipolar Disord. 2018; 20 (6): 506-514. doi: 10.1111/bdi.12638 29527766
18. Winham SJ, Cuellar-Barboza AB, Oliveros A, Genome-wide association study of bipolar disorder accounting for effect of body mass index identifies a new risk allele in TCF7L2. Mol Psychiatry. 2014; 19 (9): 1010-1016. doi: 10.1038/mp.2013.159 24322204
19. Cuellar-Barboza AB, Winham SJ, McElroy SL, Accumulating evidence for a role of TCF7L2 variants in bipolar disorder with elevated body mass index. Bipolar Disord. 2016; 18 (2): 124-135. doi: 10.1111/bdi.12368 26934194
20. Bellivier F, Golmard J-L, Rietschel M, Age at onset in bipolar I affective disorder: further evidence for three subgroups. Am J Psychiatry. 2003; 160 (5): 999-1001. doi: 10.1176/appi.ajp.160.5.999 12727708
21. Bellivier F, Etain B, Malafosse A, Age at onset in bipolar I affective disorder in the USA and Europe. World J Biol Psychiatry. 2014; 15 (5): 369-376. doi: 10.3109/15622975.2011.639801 22188366
22. Croarkin PE, Luby JL, Cercy K, Genetic risk score analysis in early-onset bipolar disorder. J Clin Psychiatry. 2017; 78 (9): 1337-1343. doi: 10.4088/JCP.15m10314 28199072
23. Goodwin FK, Jamison KR. Manic-Depressive Illness: Bipolar Disorders and Recurrent Depression. 2nd ed. New York: Oxford University Press; 2007.
24. Markota M, Coombes BJ, Larrabee BR, Association of schizophrenia polygenic risk score with manic and depressive psychosis in bipolar disorder. Transl Psychiatry. 2018; 8 (1): 188. doi: 10.1038/s41398-018-0242-3 30201969
25. Dickerson F, Stallings C, Origoni A, Antibodies to Toxoplasma gondii in individuals with mania. Bipolar Disord. 2014; 16 (2): 129-136. doi: 10.1111/bdi.12123 24102676
26. Dollard SC, Staras SAS, Amin MM, Schmid DS, Cannon MJ. National prevalence estimates for cytomegalovirus IgM and IgG avidity and association between high IgM antibody titer and low IgG avidity. Clin Vaccine Immunol. 2011; 18 (11): 1895-1899. doi: 10.1128/CVI.05228-11 21918114
27. Jones JL, Kruszon-Moran D, Elder S, Toxoplasma gondii infection in the United States, 2011-2014. Am J Trop Med Hyg. 2018; 98 (2): 551-557. doi: 10.4269/ajtmh.17-0677 29260660
28. Timpson NJ, Nordestgaard BG, Harbord RM, C-reactive protein levels and body mass index: elucidating direction of causation through reciprocal Mendelian randomization. Int J Obes (Lond). 2011; 35 (2): 300-308. doi: 10.1038/ijo.2010.137 20714329
29. Ohsawa M, Okayama A, Nakamura M, CRP levels are elevated in smokers but unrelated to the number of cigarettes and are decreased by long-term smoking cessation in male smokers. Prev Med. 2005; 41 (2): 651-656. doi: 10.1016/j.ypmed.2005.02.002 15917065
30. Fond G, Boyer L, Gaman A, Treatment with anti-toxoplasmic activity (TATA) for toxoplasma positive patients with bipolar disorders or schizophrenia: a cross-sectional study. J Psychiatr Res. 2015; 63: 58-64. doi: 10.1016/j.jpsychires.2015.02.011 25769398
31. Yolken R, Torrey EF, Dickerson F. Evidence of increased exposure to Toxoplasma gondii in individuals with recent onset psychosis but not with established schizophrenia. PLoS Negl Trop Dis. 2017;11(11):e0006040. doi: 10.1371/journal.pntd.0006040.
32. Dickerson F, Origoni A, Schweinfurth LAB, Clinical and serological predictors of suicide in schizophrenia and major mood disorders. J Nerv Ment Dis. 2018; 206 (3): 173-178. doi: 10.1097/NMD.0000000000000772 29474231
33. Ford BN, Yolken RH, Dickerson FB, Reduced immunity to measles in adults with major depressive disorder. Psychol Med. 2019; 49 (2): 243-249. doi: 10.1017/S0033291718000661 29552990
34. Fernandes BS, Steiner J, Molendijk ML, C-reactive protein concentrations across the mood spectrum in bipolar disorder: a systematic review and meta-analysis. Lancet Psychiatry. 2016; 3 (12): 1147-1156. doi: 10.1016/S2215-0366(16)30370-4 27838212
35. Griffiths P, Baraniak I, Reeves M. The pathogenesis of human cytomegalovirus. J Pathol. 2015; 235 (2): 288-297. doi: 10.1002/path.4437 25205255
36. Han D, Byun S-H, Kim J, Human cytomegalovirus IE2 protein disturbs brain development by the dysregulation of neural stem cell maintenance and the polarization of migrating neurons. J Virol. 2017;91:e00799-17. doi: 10.1128/JVI.00799-17.
37. Prusty BK, Gulve N, Govind S, Active HHV-6 infection of cerebellar purkinje cells in mood disorders. Front Microbiol. 2018; 9: 1955. doi: 10.3389/fmicb.2018.01955 30186267
38. Meesing A, Razonable RR. New developments in the management of cytomegalovirus infection after transplantation. Drugs. 2018; 78 (11): 1085-1103. doi: 10.1007/s40265-018-0943-1 29961185
39. Amsterdam JD, Maislin G, Rybakowski J. A possible antiviral action of lithium carbonate in herpes simplex virus infections. Biol Psychiatry. 1990; 27 (4): 447-453. doi: 10.1016/0006-3223(90)90555-G 2155671
40. Michaelis M, Ha TAT, Doerr HW, Cinatl J Jr. Valproic acid interferes with antiviral treatment in human cytomegalovirus-infected endothelial cells. Cardiovasc Res. 2008; 77 (3): 544-550. doi: 10.1093/cvr/cvm061 18006438
41. Pape K, Tamouza R, Leboyer M, Zipp F. Immunoneuropsychiatry-novel perspectives on brain disorders. Nat Rev Neurol. 2019; 15 (6): 317-328. doi: 10.1038/s41582-019-0174-4 30988501
42. Ford BN, Yolken RH, Aupperle RL, Association of early-life stress with cytomegalovirus infection in adults with major depressive disorder. JAMA Psychiatry. 2019; 76 (5): 545-547. doi: 10.1001/jamapsychiatry.2018.4543 30840037
43. Villard O, Breit L, Cimon B,; French National Reference Center for Toxoplasmosis Network. Comparison of four commercially available avidity tests for Toxoplasma gondii-specific IgG antibodies. Clin Vaccine Immunol. 2013; 20 (2): 197-204. doi: 10.1128/CVI.00356-12 23239801