Toxoplasmosis in a Cohort of Italian Patients With Bipolar and Psychotic Disorders: How Infection May Affect Clinical Features?
Journal
The Journal of nervous and mental disease
ISSN: 1539-736X
Titre abrégé: J Nerv Ment Dis
Pays: United States
ID NLM: 0375402
Informations de publication
Date de publication:
Feb 2020
Feb 2020
Historique:
entrez:
28
1
2020
pubmed:
28
1
2020
medline:
12
2
2020
Statut:
ppublish
Résumé
This study investigated the seroprevalence of Toxoplasma gondii in a cohort of 101 Italian inpatients affected by mood or schizophrenia-spectrum disorders and compared clinical features between seronegative and seropositive subjects. Patients diagnosed according to DSM-5 criteria underwent clinical assessments and blood collection to test parasite-specific IgG/IgM serum levels. Twenty-eight patients (27.7%) had IgG anti-T. gondii, and none had IgM antibodies. We found higher prevalence rate in patients aged 40 years or older, as compared with younger. No significant association was detected between T. gondii and a specific diagnostic category; however, bipolar disorder (BD)-II showed the highest positivity rate (40.9%). The seropositive status was significantly associated with a lower presence of psychotic symptoms, higher number of total episodes of predominant excitatory polarity, longer illness duration, and lower severity of current episode, particularly anxiety, depressive, and withdrawal/retardation symptoms. These preliminary results seem to point out an association between chronic toxoplasmosis and a specific subtype of BD.
Identifiants
pubmed: 31985560
doi: 10.1097/NMD.0000000000001102
pii: 00005053-202002000-00005
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
118-126Références
Abdollahian E, Shafiei R, Mokhber N, Kalantar K, Fata A (2017) Seroepidemiological study of Toxoplasma gondii infection among psychiatric patients in Mashhad, Northeast of Iran. Iran J Parasitol. 12:117–122.
Alvarado-Esquivel C, Sánchez-Anguiano LF, Arnaud-Gil CA, López-Longoria JC, Molina-Espinoza LF, Estrada-Martínez S, Liesenfeld O, Hernández-Tinoco J, Sifuentes-Álvarez A, Salas-Martínez C (2013) Toxoplasma gondii infection and suicide attempts: A case-control study in psychiatric outpatients. J Nerv Ment Dis. 201:948–952.
Alvarado-Esquivel C, Sanchez-Anguiano LF, Hernandez-Tinoco J, Berumen-Segovia LO, Torres-Prieto YE, Estrada-Martinez S, Perez-Alamos AR, Ortiz-Jurado MN, Molotla-de-Leon G, Beristain Garcia I, Rabago-Sanchez E, Liesenfeld O (2016) Toxoplasma gondii infection and mixed anxiety and depressive disorder: A case-control seroprevalence study in Durango, Mexico. J Clin Med Res. 8:519–523.
Alvarado-Esquivel C, Urbina-Alvarez JD, Estrada-Martinez S, Torres-Castorena A, Molotla-de-León G, Liesenfeld O, Dubey JP (2011) Toxoplasma gondii infection and schizophrenia: A case control study in a low Toxoplasma seroprevalence Mexican population. Parasitol Int. 60:151–155.
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders (5th ed). Arlington, VA: American Psychiatric Publishing.
Amminger GP, McGorry PD, Berger GE, Wade D, Yung AR, Phillips LJ, Harrigan SM, Francey SM, Yolken RH (2007) Antibodies to infectious agents in individuals at ultra-high risk for psychosis. Biol Psychiatry. 61:1215–1217.
Arling TA, Yolken RH, Lapidus M, Langenberg P, Dickerson FB, Zimmerman SA, Balis T, Cabassa JA, Scrandis DA, Tonelli LH, Postolache TT (2009) Toxoplasma gondii antibody titers and history of suicide attempts in patients with recurrent mood disorders. J Nerv Ment Dis. 197:905–908.
Bahia-Oliveira LM, Jones JL, Azevedo-Silva J, Alves CC, Oréfice F, Addiss DG (2003) Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis. 9:55–62.
Bak J, Shim SH, Kwon YJ, Lee HY, Kim JS, Yoon H, Lee YJ (2018) The association between suicide attempts and Toxoplasma gondii infection. Clin Psychopharmacol Neurosci. 16:95–102.
Barichello T, Badawy M, Pitcher MR, Saigal P, Generoso JS, Goularte JA, Simões LR, Quevedo J, Carvalho AF (2016) Exposure to perinatal infections and bipolar disorder: A systematic review. Curr Mol Med. 16:106–118.
Berenreiterova M, Flegr J, Kuběna AA, Němec P (2011) The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: Implications for the behavioral manipulation hypothesis. PLoS One. 6:e28925.
Bortolato B, Köhler CA, Evangelou E, León-Caballero J, Solmi M, Stubbs B, Belbasis L, Pacchiarotti I, Kessing LV, Berk M, Vieta E, Carvalho AF (2017) Systematic assessment of environmental risk factors for bipolar disorder: An umbrella review of systematic reviews and meta-analyses. Bipolar Disord. 19:84–96.
Burgdorf KS, Trabjerg BB, Pedersen MG, Nissen J, Banasik K, Pedersen OB, Sørensen E, Nielsen KR, Larsen MH, Erikstrup C, Bruun-Rasmussen P, Westergaard D, Thørner LW, Hjalgrim H, Paarup HM, Brunak S, Pedersen CB, Torrey EF, Werge T, Mortensen PB, Yolken RH, Ullum H (2019) Large-scale study of Toxoplasma and cytomegalovirus shows an association between infection and serious psychiatric disorders. Brain Behav Immun. 79:152–158.
Carruthers VB, Suzuki Y (2007) Effects of Toxoplasma gondii infection on the brain. Schizophr Bull. 33:745–751.
Cetinkaya Z, Yazar S, Gecici O, Namli MN (2007) Anti–Toxoplasma gondii antibodies in patients with schizophrenia—Preliminary findings in a Turkish sample. Schizophr Bull. 33:789–791.
Coccaro EF, Lee R, Kavoussi RJ (2010) Aggression, suicidality, and intermittent explosive disorder: Serotonergic correlates in personality disorder and healthy control subjects. Neuropsychopharmacology. 35:435–444.
Coccaro EF, Lee R, Vezina P (2013) Cerebrospinal fluid glutamate concentration correlates with impulsive aggression in human subjects. J Psychiatr Res. 47:1247–1253.
Cook TB, Brenner LA, Cloninger CR, Langenberg P, Igbide A, Giegling I, Hartmann AM, Konte B, Friedl M, Brundin L, Groer MW, Can A, Rujescu D, Postolache TT (2015) "Latent" infection with Toxoplasma gondii: Association with trait aggression and impulsivity in healthy adults. J Psychiatr Res. 60:87–94.
Del Grande C, Contini C, Schiavi E, Rutigliano G, Maritati M, Seraceni S, Pinto B, Dell'Osso L, Bruschi F (2017a) Bipolar disorder with psychotic features and ocular toxoplasmosis: A possible pathogenetic role of the parasite? J Nerv Ment Dis. 205:192–195.
Del Grande C, Galli L, Schiavi E, Dell'Osso L, Bruschi F (2017b) Is Toxoplasma gondii a trigger of bipolar disorder? Pathogens. 6:pii: E3.
Dickerson F, Stallings C, Origoni A, Katsafanas E, Schweinfurth L, Savage C, Khushalani S, Yolken R (2014) Antibodies to Toxoplasma gondii and cognitive functioning in schizophrenia, bipolar disorder, and nonpsychiatric controls. J Nerv Ment Dis. 202:589–593.
Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol. 38:1257–1278.
Dunn AJ (2006) Effects of cytokines and infections on brain neurochemistry. Clin Neurosci Res. 6:52–68.
Esshili A, Thabet S, Jemli A, Trifa F, Mechri A, Zaafrane F, Gaha L, Juckel G, Babba H, Bel Hadj Jrad B (2016) Toxoplasma gondii infection in schizophrenia and associated clinical features. Psychiatry Res. 245:327–332.
Fabiani S, Pinto B, Bonuccelli U, Bruschi F (2015) Neurobiological studies on the relationship between toxoplasmosis and neuropsychiatric diseases. J Neurol Sci. 351:3–8.
First MB, Williams JBW, Karg RS, Spitzer RL (2015) Structured Clinical Interview for DSM-5—Research Version (SCID-5 for DSM-5, Research Version; SCID-5-RV, Version 1.0.0). Arlington, VA: American Psychiatric Association.
Flegr J (2007) Effects of Toxoplasma on human behaviour. Schizophr Bull. 33:757–760.
Flegr J (2013a) Influence of latent Toxoplasma infection on human personality, physiology and morphology: Pros and cons of the Toxoplasma-human model in studying the manipulation hypothesis. J Exp Biol. 216(pt 1):127–133.
Flegr J (2013b) How and why Toxoplasma makes us crazy. Trends Parasitol. 29:156–163.
Flegr J, Prandota J, Sovičková M, Israili ZH (2014) Toxoplasmosis—A global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS One. 9:e90203.
Freedman D, Bao Y, Shen L, Schaefer CA, Brown AS (2016) Maternal T. gondii, offspring bipolar disorder and neurocognition. Psychiatry Res. 243:382–389.
Galli L, Del Grande C, Rindi L, Mangia C, Mangano V, Schiavi E, Masci I, Pinto B, Kramer L, Dell'Osso L, Bruschi F (2019) Lack of circulating Toxoplasma gondii DNA in seropositive patients with bipolar or schizophrenia spectrum disorders. Psychiatry Res. 273:706–711.
Gatkowska J, Wieczorek M, Dziadek B, Dzitko K, Dlugonska H (2012) Behavioral changes in mice caused by Toxoplasma gondii invasion of brain. Parasitol Res. 111:53–58.
Gelaye W, Kebede T, Hailu A (2015) High prevalence of anti-Toxoplasma antibodies and absence of Toxoplasma gondii infection risk factors among pregnant women attending routine antenatal care in two Hospitals of Addis Ababa, Ethiopia. Int J Infect Dis. 34:41–45.
Goodwin DG, Strobl J, Mitchell SM, Zajac AM, Lindsay DS (2008) Evaluation of the mood-stabilizing agent valproic acid as a preventative for toxoplasmosis in mice and activity against tissue cysts in mice. J Parasitol. 94:555–557.
Guy W (Ed) (1976) ECDEU Assessment Manual for Psychopharmacology (pp 218–222). US Department of Health, Education, and Welfare publication (ADM) 76–338. Rockville, MD: National Institute of Mental Health.
Hamdani N, Daban-Huard C, Lajnef M, Gadel R, Le Corvoisier P, Delavest M, Carde S, Lépine JP, Jamain S, Houenou J, Galeh B, Richard JR, Aoki M, Charron D, Krishnamoorthy R, Yolken R, Dickerson F, Tamouza R, Leboyer M (2015) Cognitive deterioration among bipolar disorder patients infected by Toxoplasma gondii is correlated to interleukin 6 levels. J Affect Disord. 179:161–166.
Hamdani N, Daban-Huard C, Lajnef M, Richard JR, Delavest M, Godin O, Le Guen E, Vederine FE, Lépine JP, Jamain S, Houenou J, Le Corvoisier P, Aoki M, Moins-Teisserenc H, Charron D, Krishnamoorthy R, Yolken R, Dickerson F, Tamouza R, Leboyer M (2013) Relationship between Toxoplasma gondii infection and bipolar disorder in a French sample. J Affect Disord. 148:444–448.
Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry. 23:56–62.
Hinze-Selch D, Däubener W, Eggert L, Erdag S, Stoltenberg R, Wilms S (2007) A controlled prospective study of Toxoplasma gondii infection in individuals with schizophrenia: Beyond seroprevalence. Schizophr Bull. 33:782–788.
Hofhuis A, van Pelt W, van Duynhoven YT, Nijhuis CD, Mollema L, van der Klis FR, Havelaar AH, Kortbeek LM (2011) Decreased prevalence and age-specific risk factors for Toxoplasma gondii IgG antibodies in The Netherlands between 1995/1996 and 2006/2007. Epidemiol Infect. 139:530–538.
Jones JL, Dargelas V, Roberts J, Press C, Remington JS, Montoya JG (2009) Risk factors for Toxoplasma gondii infection in the United States. Clin Infect Dis. 49:878–884.
Jones JL, Kruszon-Moran D, Elder S, Rivera HN, Press C, Montoya JG, McQuillan GM (2018) Toxoplasma gondii infection in the United States, 2011–2014. Am J Trop Med Hyg. 98:551–557.
Jones-Brando L, Torrey EF, Yolken R (2003) Drugs used in the treatment of schizophrenia and bipolar disorder inhibit the replication of Toxoplasma gondii. Schizophr Res. 62:237–244.
Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 13:261–276.
Leweke FM, Gerth CW, Koethe D, Klosterkötter J, Ruslanova I, Krivogorsky B, Torrey EF, Yolken RH (2004) Antibodies to infectious agents in individuals with recent onset schizophrenia. Eur Arch Psychiatry Clin Neurosci. 254:4–8.
Ling VJ, Lester D, Mortensen PB, Langenberg PW, Postolache TT (2011) Toxoplasma gondii seropositivity and suicide rates in women. J Nerv Ment Dis. 199:440–444.
Markovitz AA, Simanek AM, Yolken RH, Galea S, Koenen KC, Chen S, Aiello AE (2015) Toxoplasma gondii and anxiety disorders in a community-based sample. Brain Behav Immun. 43:192–197.
McConkey GA, Martin HL, Bristow GC, Webster JP (2013) Toxoplasma gondii infection and behaviour - location, location, location? J Exp Biol. 216(pt 1):113–119.
Montoya JG, Liesenfeld O (2004) Toxoplasmosis. Lancet. 363:1965–1976.
Morosini PL, Magliano L, Brambilla L, Ugolini S, Pioli R (2000) Development, reliability and acceptability of a new version of the DSM-IV Social and Occupational Functioning Assessment Scale (SOFAS) to assess routine social functioning. Acta Psychiatr Scand. 101:323–329.
Mosti M, Pinto B, Giromella A, Fabiani S, Cristofani R, Panichi M, Bruschi F (2013) A 4-year evaluation of toxoplasmosis seroprevalence in the general population and in women of reproductive age in central Italy. Epidemiol Infect. 141:2192–2195.
Oliveira J, Kazma R, Le Floch E, Bennabi M, Hamdani N, Bengoufa D, Dahoun M, Manier C, Bellivier F, Krishnamoorthy R, Deleuze JF, Yolken R, Leboyer M, Tamouza R (2016) Toxoplasma gondii exposure may modulate the influence of TLR2 genetic variation on bipolar disorder: A gene-environment interaction study. Int J Bipolar Disord. 4:11.
Omar A, Bakar OC, Adam NF, Osman H, Osman A, Suleiman AH, Manaf MR, Selamat MI (2015) Seropositivity and serointensity of Toxoplasma gondii antibodies and DNA among patients with schizophrenia. Korean J Parasitol. 53:29–34.
Overall JE, Gorham DR (1962) The Brief Psychiatric Rating Scale. Psychol Rep. 10:799–812.
Parlog A, Schluter D, Dunay IR (2015) Toxoplasma gondii-induced neuronal alterations. Parasite Immunol. 37:159–170.
Pearce BD, Kruszon-Moran D, Jones JL (2012) The relationship between Toxoplasma gondii infection and mood disorders in the third National Health and Nutrition Survey. Biol Psychiatry. 72:290–295.
Pedersen MG, Mortensen PB, Nørgaard-Pedersen B, Postolache TT (2012) Toxoplasma gondii infection and self-directed violence in mothers. Arch Gen Psychiatry. 69:1123–1130.
Pedersen MG, Stevens H, Pedersen CB, Nørgaard-Pedersen B, Mortensen PB (2011) Toxoplasma infection and later development of schizophrenia in mothers. Am J Psychiatry. 168:814–821.
Pinto B, Castagna B, Mattei R, Bruzzi R, Chiumiento L, Cristofani R, Buffolano W, Bruschi F (2012) Seroprevalence for toxoplasmosis in individuals living in North West Tuscany: Access to Toxo-test in central Italy. Eur J Clin Microbiol Infect Dis. 31:1151–1156.
Pinto B, Mattei R, Moscato GA, Cristofano M, Giraldi M, Scarpato R, Buffolano W, Bruschi F (2017) Toxoplasma infection in individuals in central Italy: Does a gender-linked risk exist? Eur J Clin Microbiol Infect Dis. 36:739–746.
Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, McConkey GA (2011) The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS One. 6:e23866.
Remington JS, McLeod R, Thulliez P, Desmonts G (2001) Toxoplasmosis. In Remington JS, Klein J (Eds), Infectious diseases of the fetus and newborn infant (5th ed, pp 205–346). Philadelphia, PA: WB Saunders.
Robert-Gangneux F, Dardé ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 25:264–296.
Sanches M, Keshavan MS, Brambilla P, Soares JC (2008) Neurodevelopmental basis of bipolar disorder: A critical appraisal. Prog Neuropsychopharmacol Biol Psychiatry. 32:1617–1627.
Sinai AP, Watts EA, Dhara A, Murphy RD, Gentry MS, Patwardhan A (2016) Re-examining chronic Toxoplasma gondii infection: Surprising activity for a "dormant" parasite. Curr Clin Microbiol Rep. 3:175–185.
Song J, Bergen SE, Kuja-Halkola R, Larsson H, Landen M, Lichtenstein P (2015) Bipolar disorder and its relation to major psychiatric disorders: A family-based study in the Swedish population. Bipolar Disord. 17:184–193.
Sugden K, Moffitt TE, Pinto L, Poulton R, Williams BS, Caspi A (2016) Is Toxoplasma gondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLoS One. 11:e0148435.
Sutterland AL, Fond G, Kuin A, Koeter MW, Lutter R, van Gool T, Yolken R, Szoke A, Leboyer M, de Haan L (2015) Beyond the association. Toxoplasma gondii in schizophrenia, bipolar disorder, and addiction: Systematic review and meta-analysis. Acta Psychiatr Scand. 132:161–179.
Suvisaari J, Torniainen-Holm M, Lindgren M, Härkänen T, Yolken RG (2017) Toxoplasma gondii infection and common mental disorders in the Finnish general population. J Affect Disord. 223:20–25.
Tedla Y, Shibre T, Ali O, Tadele G, Woldeamanuel Y, Asrat D, Aseffa A, Mihret W, Abebe M, Alem A, Medhin G, Habte A (2011) Serum antibodies to Toxoplasma gondii and Herpesvidae family viruses in individuals with schizophrenia and bipolar disorder: A case-control study. Ethiop Med J. 49:211–220.
Torrey EF, Bartko JJ, Lun ZR, Yolken RH (2007) Antibodies to Toxoplasma gondii in patients with schizophrenia: A meta-analysis. Schizophr Bull. 33:729–736.
Torrey EF, Bartko JJ, Yolken RH (2012) Toxoplasma gondii and other risk factors for schizophrenia: An update. Schizophr Bull. 38:642–647.
Wang HL, Wang GH, Li QY, Shu C, Jiang MS, Guo Y (2006) Prevalence of Toxoplasma infection in first-episode schizophrenia and comparison between Toxoplasma-seropositive and Toxoplasma-seronegative schizophrenia. Acta Psychiatr Scand. 114:40–48.
Webster JP, Lamberton PH, Donnelly CA, Torrey EF (2006) Parasites as causative agents of human affective disorders? The impact of anti-psychotic, mood-stabilizer and anti-parasite medication on Toxoplasma gondii's ability to alter host behaviour. Proc Biol Sci. 273:1023–1030.
Weiss LM, Dubey JP (2009) Toxoplasmosis: A history of clinical observations. Int J Parasitol. 39:895–901.
Xiao J, Jones-Brando L, Talbot CC Jr., Yolken RH (2011) Differential effects of three canonical Toxoplasma strains on gene expression in human neuroepithelial cells. Infect Immun. 79:1363–1373.
Yolken RH, Dickerson FB, Fuller Torrey E (2009) Toxoplasma and schizophrenia. Parasite Immunol. 31:706–715.
Yolken R, Torrey EF, Dickerson F (2017) Evidence of increased exposure to Toxoplasma gondii in individuals with recent onset psychosis but not with established schizophrenia. PLoS Negl Trop Dis. 11:e0006040.
Young RC, Biggs JT, Ziegler VE, Meyer DA (1978) A rating scale for mania: Reliability, validity and sensitivity. Br J Psychiatry. 133:429–435.