Folia Parasitologica 65:011 (2018) | DOI: 10.14411/fp.2018.011
Toxoplasma gondii seropositivity and substance use in US adults
- 1 Department of Psychology, Brigham Young University, Provo, Utah, United States of America;
- 2 The Neuroscience Center, Brigham Young University, Provo, Utah, United States of America;
- 3 Department of Sociology, Brigham Young University, Provo, Utah, United States of America;
- 4 Department of Public Health, Brigham Young University, Provo, Utah, United States of America This article contains supporting information (S1) online at http://folia.paru.cas.cz/suppl/2018-65-011.pdf
The intracellular parasite Toxoplasma gondii (Nicolle et Manceaux, 1908) infects humans resulting in acute toxoplasmosis, an infection that in immunocompetent people is typically mild but results in persistent latent toxoplasmosis. In that T. gondii appears to affect dopamine synthesis and because addicting drugs affect midbrain dopamine transmission, latent toxoplasmosis could influence substance use. Using both the third and continuous National Health and Nutrition Examination Surveys from the US Centers for Disease Control and Prevention, we used logistic regression to test for associations between T. gondii seropositivity and subject self-report of having ever used tobacco, alcohol, marijuana, cocaine, heroin, or methamphetamine. In the third NHANES dataset, which included data for tobacco, alcohol, marijuana and cocaine, T. gondii seropositivity was associated with a reduced likelihood of self-reported marijuana (OR = 0.71 [95% CI: 0.58; 0.87]; p = 0.001) and cocaine use (OR = 0.72 [95% CI: 0.56; 0.91]; p = 0.006). In the continuous National Health and Nutrition Examination Surveys dataset, which included data for all six substances, T. gondii seropositivity was associated with a reduced likelihood of self-reported tobacco (OR = 0.87 [95% CI: 0.76; 1.00]; p = 0.044), marijuana (OR = 0.60 [95% CI: 0.50; 0.72]; p < 0.001), heroin (OR = 0.60 [95% CI: 0.42; 0.85]; p = 0.005) and methamphetamine use (OR = 0.54 [95% CI: 0.38; 0.77]; p = 0.001). We observed interactions between sex and T. gondii seropositivity in the prediction of self-reported use of tobacco and alcohol. Further, T. gondii seropositivity appeared to remove the protective effect of education and economic status against self-reported cigarette smoking. These findings suggest that T. gondii seropositivity may be inversely associated with some but not all types of substance use in US adults.
Keywords: Toxoplasmosis, tobacco, alcohol, marijuana, cocaine, heroin, methamphetamine, drug use
Received: May 4, 2017; Accepted: June 29, 2018; Published online: September 10, 2018 Show citation
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References
- Adinoff B. 2004: Neurobiologic processes in drug reward and addiction. Harv. Rev. Psychiatry 12: 305-320.
Go to original source...
Go to PubMed... - Alvarado-Esquivel C., Carrillo-Oropeza D., Pacheco-Vega S.J., Hernández-Tinoco J., Salcedo-Jaquez M., Sánchez-Anguiano L.F., Ortiz-Jurado M.N., Alarcón-Alvarado Y., Liesenfeld O., Beristain-García I. 2015: Toxoplasma gondii exposure in patients suffering from mental and behavioural disorders due to psychoactive substance use. BMC Infect. Dis. 15: 172.
Go to original source...
Go to PubMed... - Cabral C.M., Tuladhar S., Dietrich H.K., Nguyen E., Macdonald W.R., Trivedi T., Devineni A., Koshy A.A. 2016: Neurons are the primary target cell for the brain-tropic intracellular parasite Toxoplasma gondii. PLoS Pathog. 12: e1005447.
Go to original source...
Go to PubMed... - Carruthers V.B., Suzuki Y. 2007: Effects of Toxoplasma gondii infection on the brain. Schizophr. Bull. 33: 745-751.
Go to original source...
Go to PubMed... - Centers for Disease Control and Prevention 2011: Analytic note regarding 2007-2010 survey design changes and combining data across other survey cycles. Available from: http://www.cdc.gov/nchs/data/nhanes/analyticnote_2007-2010.pdf.
- Cook T.B., Brenner L.A., Cloninger C.R., Langenberg P., Igbide A., Giegling I., Hartmann A.M., Konte B., Friedl M., Brundin L., Groer M.W., Can A., Rujescu D., Postolache T.T. 2015: "Latent" infection with Toxoplasma gondii: association with trait aggression and impulsivity in healthy adults. J. Psychiatr. Res. 60: 87-94.
Go to original source...
Go to PubMed... - Devoto P., Fattore L., Antinori S., Saba P., Frau R., Fratta W., Gessa G.L. 2016: Elevated dopamine in the medial prefrontal cortex suppresses cocaine seeking via D1 receptor overstimulation. Addict. Biol. 21: 61-71.
Go to original source...
Go to PubMed... - Dupont C.D., Christian D.A., Hunter C.A. 2012: Immune response and immunopathology during toxoplasmosis. Semin. Immunopathol. 34: 793-813.
Go to original source...
Go to PubMed... - Elmore S.A., Jones J.L., Conrad P.A., Patton S., Lindsay D.S., Dubey J.P. 2010: Toxoplasma gondii: epidemiology, feline clinical aspects and prevention. Trends Parasitol. 26: 190-196.
Go to original source...
Go to PubMed... - 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.
Go to original source...
Go to PubMed... - Flegr J. 2013: 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: 127-133.
Go to original source...
Go to PubMed... - Flegr J. 2015: Neurological and neuropsychiatric consequences of chronic Toxoplasma infection. Curr. Clin. Microbiol. Rep. 2: 163-172.
Go to original source... - Flegr J., Kodym P., Tolarová V. 2000: Correlation of duration of latent Toxoplasma gondii infection with personality changes in women. Biol. Psychol. 53: 57-68.
Go to original source...
Go to PubMed... - Flegr J., Prandota J., Sovičková M., Israili Z.H. 2014: Toxoplasmosis - a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PloS ONE 9: e90203.
Go to original source...
Go to PubMed... - Flegr J., Preiss M., Klose J., Havlíček J., Vitáková M., Kodym P. 2003: Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii dopamine, a missing link between schizophrenia and toxoplasmosis? Biol. Psychol. 63: 253-268.
Go to original source...
Go to PubMed... - Frank M.J., O'Reilly R.C. 2006: A mechanistic account of striatal dopamine function in human cognition: Psychopharmacological studies with cabergoline and haloperidol. Behav. Neurosci. 120: 497-517.
Go to original source...
Go to PubMed... - Gunter E.W., Lewis B.G., Koncikowski S.M. 1996: Laboratory Procedures Used for the Third National Health and Nutrition Examination Survey (NHANES III), 1988-1994. U.S. Department of Health and Human Services, VII-SS-15 pp.
- Hartka E., Fillmore K.M. 1989: Cross-cultural and cross-temporal explanations of drinking behaviour: contributions from epidemiology, life-span developmental psychology and the sociology of aging. Br. J. Addict. 84: 1409-1417.
Go to original source...
Go to PubMed... - Hermes G., Ajioka J.W., Kelly K.A., Mui E., Roberts F., Kasza K., Mayr T., Kirisits M.J., Wollmann R., Ferguson D.J., Roberts C.W., Hwang J.H., Trendler T., Kennan R.P., Suzuki Y., Reardon C., Hickey W.F., Chen L., Mcleod R. 2008: Neurological and behavioural abnormalities, ventricular dilatation, altered cellular functions, inflammation and neuronal injury in brains of mice due to common, persistent, parasitic infection. J. Neuroinflammation 5: 48.
Go to original source...
Go to PubMed... - Higgins S.T., Kurti A.N., Redner R., White T.J., Keith D.R., Gaalema D.E., Sprague B.L., Stanton C.A., Roberts M.E., Doogan N.J., Priest J.S. 2016: co-occurring risk factors for current cigarette smoking in a U.S. nationally representative sample. Prev. Med. 92: 110-117.
Go to original source...
Go to PubMed... - Hill D.E., Sreekumar C., Jones J., Dubey J.P. 2007: Toxoplasma gondii. In S. Simjee (Ed.), Foodborne Diseases. Humana Press, New Jersey, pp. 337-353.
Go to original source... - Hinze-Selch D., Daubener 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.
Go to original source...
Go to PubMed... - Jones J.L., Kruszon-Moran D., Rivera H.N., Price C., Wilkins P.P. 2014: Toxoplasma gondii seroprevalence in the United States 2009-2010 and comparison with the past two decades. Am. J. Trop. Med. Hyg. 90: 1135-1139.
Go to original source...
Go to PubMed... - Lindová J., Kuběna A.A., Šturcová, H., Křivohlavá R., Novotná M., Rubešová A., Havlíček J., Kodym P., Flegr J. 2010: Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii induced behavioural changes. Folia Parasitol. 57: 136-142.
Go to original source...
Go to PubMed... - Maralani V. 2013: Educational inequalities in smoking: the role of initiation versus quitting. Soc. Sci. Med. 84: 129-137.
Go to original source...
Go to PubMed... - Martin H.L., Alsaady I., Howell G., Prandovszky E., Peers C., Robinson P., McConkey G.A. 2015: Effect of parasitic infection on dopamine biosynthesis in dopaminergic cells. Neuroscience 306: 50-62.
Go to original source...
Go to PubMed... - McConkey G.A., Martin H.L., Bristow G.C., Webster J.P. 2013: Toxoplasma gondii infection and behaviour - location, location, location? J. Exp. Biol. 216: 113-119.
Go to original source...
Go to PubMed... - Mortensen P.B., Norgaard-Pedersen B., Waltoft B.L., Sorensen T.L., Hougaard D., Yolken R.H. 2007: Early infections of Toxoplasma gondii and the later development of schizophrenia. Schizophr. Bull. 33: 741-744.
Go to original source...
Go to PubMed... - Noble E.P. 2000: Addiction and its reward process through polymorphisms of the D2 dopamine receptor gene: a review. Eur. Psychiatry 15: 79-89.
Go to original source...
Go to PubMed... - Nutt D.J., Lingford-Hughes A., Erritzoe D., Stokes P.R. 2015: The dopamine theory of addiction: 40 years of highs and lows. Nat. Rev. Neurosci. 16: 305-312.
Go to original source...
Go to PubMed... - Okusaga O., Duncan E., Langenberg P., Brundin L., Fuchs D., Groer M.W., Giegling I., Stearns-Yoder K.A., Hartmann A.M., Konte B., Friedl M., Brenner L.A., Lowry C.A., Rujescu D., Postolache T.T. 2016: Combined Toxoplasma gondii seropositivity and high blood kynurenine-linked with nonfatal suicidal self-directed violence in patients with schizophrenia. J. Psychiatr. Res. 72: 74-81.
Go to original source...
Go to PubMed... - Payer D., Balasubramaniam G., Boileau I. 2014: What is the role of the D3 receptor in addiction? A mini review of pet studies with [(11)C]-(+)-PHNO. Prog. Neuropsychopharmacol. Biol. Psychiatry 52: 4-8.
Go to original source...
Go to PubMed... - Pedersen M.G., Mortensen P.B., Norgaard-Pedersen B., Postolache T.T. 2012: Toxoplasma gondii infection and self-directed violence in mothers. Arch. Gen. Psychiatry 69: 1123-1130.
Go to original source...
Go to PubMed... - Pine A., Shiner T., Seymour B., Dolan R.J. 2010: Dopamine, time and impulsivity in humans. J. Neurosci. 30(26): 8888-8896.
Go to original source...
Go to PubMed... - Prandovszky E., Gaskell E., Martin H., Dubey J.P., Webster J.P., McConkey G.A. 2011: The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PloS ONE 6: e23866.
Go to original source...
Go to PubMed... - Ramdani C., Carbonnell L., Vidal F., Béranger C., Dagher A., Hasbroucq T. 2015: Dopamine precursors depletion impairs impulse control in healthy volunteers. Psychopharmacology (Berl) 232: 477-487.
Go to original source...
Go to PubMed... - Schultz W. 2007: Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30: 259-288.
Go to original source...
Go to PubMed... - Skallová A., Novotná M., Kolbeková P., Gašová Z., Veselý V., Sechovská M., Flegr J. 2005: Decreased level of novelty seeking in blood donors infected with Toxoplasma. Neuro Endocrinol. Lett. 26: 480-486.
Go to PubMed... - Statacorp, Stata statistical software: Release 14, 2015: StataCorp LP: College Station, TX.
- Stock A.K., Heintschel von Heinegg E., Köhling H.L., Beste C. 2014: Latent Toxoplasma gondii infection leads to improved action control. Brain Behav. Immun. 37: 103-108.
Go to original source...
Go to PubMed... - Sutterland A.L., Fond G., Kuin A., Koeter M.W.J., 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.
Go to original source...
Go to PubMed... - Torrey E.F., Bartko J.J., Lun Z.R., Yolken R.H. 2007: Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr. Bull. 33: 729-736.
Go to original source...
Go to PubMed... - Trifilieff P., Martinez D. 2014a: Blunted dopamine release as a biomarker for vulnerability for substance use disorders. Biol. Psychiatry 76: 4-5.
Go to original source...
Go to PubMed... - Trifilieff P., Martinez D. 2014b: Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity. Neuropharmacology 76 Pt B: 498-509.
Go to original source...
Go to PubMed... - Vanyukov M.M., Nimgaonkar V.L., Kirisci L., Kirillova G.P., Reynolds M.D., Prasad K., Tarter R.E., Yolken R.H. 2017: Association of cognitive function and liability to addiction with childhood herpesvirus infections: a prospective cohort study. Dev. Psychopathol. 30: 143-152.
Go to original source...
Go to PubMed... - Wang Z.T., Harmon S., O'Malley K.L., Sibley L.D. 2015: Reassessment of the role of aromatic amino acid hydroxylases and the effect of infection by Toxoplasma gondii on host dopamine. Infect. Immun. 83: 1039-1047.
Go to original source...
Go to PubMed... - Xiao J., Li Y., Prandovszky E., Karuppagounder S.S., Talbot Jr. C.C., Dawson V.L., Dawson T.M., Yolken R.H. 2014: Microrna-132 dysregulation in Toxoplasma gondii infection has implications for dopamine signaling pathway. Neuroscience 268: 128-138.
Go to original source...
Go to PubMed... - Xiao J., Yolken R.H. 2015: Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol. 213: 828-845.
Go to original source...
Go to PubMed...


