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Association between latent toxoplasmosis and cognition in adults: a cross-sectional study

  • S. D. GALE (a1) (a2), B. L. BROWN (a1), L. D. ERICKSON (a3), A. BERRETT (a1) and D. W. HEDGES (a1) (a2)...

Summary

Latent infection from Toxoplasma gondii (T. gondii) is widespread worldwide and has been associated with cognitive deficits in some but not all animal models and in humans. We tested the hypothesis that latent toxoplasmosis is associated with decreased cognitive function in a large cross-sectional dataset, the National Health and Nutrition Examination Survey (NHANES). There were 4178 participants aged 20–59 years, of whom 19·1% had IgG antibodies against T. gondii. Two ordinary least squares (OLS) regression models adjusted for the NHANES complex sampling design and weighted to represent the US population were estimated for simple reaction time, processing speed and short-term memory or attention. The first model included only main effects of latent toxoplasmosis and demographic control variables, and the second added interaction terms between latent toxoplasmosis and the poverty-to-income ratio (PIR), educational attainment and race-ethnicity. We also used multivariate models to assess all three cognitive outcomes in the same model. Although the models evaluating main effects only demonstrated no association between latent toxoplasmosis and the cognitive outcomes, significant interactions between latent toxoplasmosis and the PIR, between latent toxoplasmosis and educational attainment, and between latent toxoplasmosis and race-ethnicity indicated that latent toxoplasmosis may adversely affect cognitive function in certain groups.

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Corresponding author

* Corresponding author: Psychology Department and Neuroscience Center, Brigham Young University, 1060 SWKT, Provo, Utah 84602, USA. E-mail: shawn_gale@byu.edu

References

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Alvarado-Esquivel, C., Liesenfeld, O., Marquez-Conde, J. A., Estrada-Martinez, S. and Dubey, J. P. (2010). Seroepidemiology of infection with Toxoplasma gondii in workers occupationally exposed to water, sewage, and soil in Durango, Mexico. Journal of Parasitology 96, 847850.
Alvarado-Esquivel, C., Torres-Castorena, A., Liesenfeld, O., Estrada-Martinez, S. and Urbina-Alvarez, J. D. (2012). High seroprevalence of Toxoplasma gondii infection in a subset of Mexican patients with work accidents and low socioeconomic status. Parasites and Vectors 5, 13.
Alvarado-Esquivel, C., Pacheco-Vega, S. J., Hernandez-Tinoco, J., Sanchez-Anguiano, L. F., Berumen-Segovia, L. O., Rodriguez-Acevedo, F. J., Beristain-Garcia, I., Rabago-Sanchez, E., Liesenfeld, O., Campillo-Ruiz, F. and Guereca-Garcia, O. A. (2014). Seroprevalence of Toxoplasma gondii infection and associated risk factors in Huicholes in Mexico. Parasites and Vectors 7, 301.
Baker, E. L., Letz, R. E., Fidler, A. T., Shalat, S., Plantamura, D. and Lyndon, M. (1985). A computer-based neurobehavioral evaluation system for occupational and environmental epidemiology: methodology and validation studies. Neurobehavioral Toxicology and Teratology 7, 369377.
Berenreiterova, M., Flegr, J., Kubena, A. A. and Nemec, 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.
Beste, C., Getzmann, S., Gajewski, P. D., Golka, K. and Falkenstein, M. (2014). Latent Toxoplasma gondii infection leads to deficits in goal-directed behavior in healthy elderly. Neurobiology of Aging 35, 10371044.
Carruthers, V. B. and Suzuki, Y. (2007). Effects of Toxoplasma gondii infection on the brain. Schizophrenia Bulletin 33, 745751.
Eppig, C., Fincher, C. L. and Thornhill, R. (2010). Parasite prevalence and the worldwide distribution of cognitive ability. Proceedings: Biological Sciences 277, 38013808.
Flegr, J., Preiss, M., Klose, J., Havlíček, J., Vitáková, M. and 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? Biological Psychology 63, 253268.
Flegr, J., Guenter, W., Bielinski, M., Deptula, A., Zalas-Wiecek, P., Piskunowicz, M., Szwed, K., Bucinski, A., Gospodarek, E. and Borkowska, A. (2012). Toxoplasma gondii infection affects cognitive function – corrigendum. Folia Parasitologica 59, 253254.
Fuks, J. M., Arrighi, R. B., Weidner, J. M., Kumar Mendu, S., Jin, Z., Wallin, R. P., Rethi, B., Birnir, B. and Barragan, A. (2012). GABAergic signaling is linked to a hypermigratory phenotype in dendritic cells infected by Toxoplasma gondii . PLoS Pathogens 8, e1003051.
Gajewski, P. D., Falkenstein, M., Hengstler, J. G. and Golka, K. (2014). Toxoplasma gondii impairs memory in infected seniors. Brain, Behavior, and Immunity 36, 193199.
Guenter, W., Bielinski, M., Deptula, A., Zalas-Wiecek, P., Piskunowicz, M., Szwed, K., Bucinski, A., Gospodarek, E. and Borkowska, A. (2012). Does Toxoplasma gondii infection affect cognitive function? A case control study. Folia Parasitologica 59, 9398.
Gulinello, M., Acquarone, M., Kim, J. H., Spray, D. C., Barbosa, H. S., Sellers, R., Tanowitz, H. B. and Weiss, L. M. (2010). Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes and Infection 12, 528537.
Havlicek, J., Gasova, Z. G., Smith, A. P., Zvara, K. and Flegr, J. (2001). Decrease of psychomotor performance in subjects with latent'asymptomatic' toxoplasmosis. Parasitology 122, 515520.
Hinze-Selch, D., Daubener, W., Eggert, L., Erdag, S., Stoltenberg, R. and Wilms, S. (2007). A controlled prospective study of Toxoplasma gondii infection in individuals with schizophrenia: beyond seroprevalence. Schizophrenia Bulletin 33, 782788.
Ingram, W. M., Goodrich, L. M., Robey, E. A. and Eisen, M. B. (2013). Mice infected with low-virulence strains of Toxoplasma gondii lose their innate aversion to cat urine, even after extensive parasite clearance. PLoS ONE 8, e75246.
Kannan, G. and Pletnikov, M. V. (2012). Toxoplasma gondii and cognitive deficits in schizophrenia: an animal model perspective. Schizophrenia Bulletin 38, 11551161.
Kaplan, G. A., Turrell, G., Lynch, J. W., Everson, S. A., Helkala, E. L. and Salonen, J. T. (2001). Childhood socioeconomic position and cognitive function in adulthood. International Journal of Epidemiology 30, 256263.
Krieg, E. F. Jr., Chrislip, D. W., Letz, R. E., Otto, D. A., Crespo, C. J., Brightwell, W. S. and Ehrenberg, R. L. (2001). Neurobehavioral test performance in the third National Health and Nutrition Examination Survey. Neurotoxicology and Teratology 23, 569589.
Kusbeci, O. Y., Miman, O., Yaman, M., Aktepe, O. C. and Yazar, S. (2011). Could Toxoplasma gondii have any role in Alzheimer disease? Alzheimer Disease and Associated Disorders 25, 13.
Letz, R. E. and Baker, E. L. (1988). NES 2: Neurobehavioral Evaluation System Manual. Neurobehavioral Systems, Inc., Winchester, MA, USA.
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., Nishino, T. and Barch, D. (2013). The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatrics 167, 11351142.
McConkey, G. A., Martin, H. L., Bristow, G. C. and Webster, J. P. (2013). Toxoplasma gondii infection and behaviour – location, location, location? Journal of Experimental Biology 216, 113119.
Miman, O., Mutlu, E. A., Ozcan, O., Atambay, M., Karlidag, R. and Unal, S. (2010). Is there any role of Toxoplasma gondii in the etiology of obsessive-compulsive disorder? Psychiatry Research 177, 263265.
Mizgajska-Wiktor, H., Jarosz, W., Andrzejewska, I., Krzykala, M., Janowski, J. and Kozlowska, M. (2013). Differences in some developmental features between Toxoplasma gondii-seropositive and seronegative school children. Folia Parasitologica 60, 416424.
Mody, P., Gupta, A., Bikdeli, B., Lampropulos, J. F. and Dharmarajan, K. (2012). Most important articles on cardiovascular disease among racial and ethnic minorities. Circulation: Cardiovascular Quality and Outcomes 5, e33e41.
Montoya, J. G. and Liesenfeld, O. (2004). Toxoplasmosis. Lancet 363, 19651976.
Pearce, B. D., Kruszon-Moran, D. and Jones, J. L. (2014). The association of Toxoplasma gondii infection with neurocognitive deficits in a population-based analysis. Social Psychiatry and Psychiatric Epidemiology 49, 10011010.
Prandovszky, E., Gaskell, E., Martin, H., Dubey, J. P., Webster, J. P. and McConkey, G. A. (2011). The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6, e23866.
Rencher, A. C. and Scott, D. T. (1990). Assessing the contribution of individual variables following rejection of a multivariate hypothesis. Communications in Statistics-Simulation and Computation 19, 535553.
Roe, C. M., Mintun, M. A., D'Angelo, G., Xiong, C., Grant, E. A. and Morris, J. C. (2008). Alzheimer disease and cognitive reserve: variation of education effect with carbon 11-labeled Pittsburgh Compound B uptake. Archives of Neurology 65, 14671471.
Stibbs, H. H. (1985). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Annals of Tropical Medicine and Parasitology 79, 153157.
Thornhill, R. and Fincher, C. L. (2011). Parasite stress promotes homicide and child maltreatment. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 366, 34663477.
Turrell, G., Lynch, J. W., Kaplan, G. A., Everson, S. A., Helkala, E. L., Kauhanen, J. and Salonen, J. T. (2002). Socioeconomic position across the lifecourse and cognitive function in late middle age. Journals of Gerontology. Series B, Psychological Sciences and Social Sciences 57, S43S51.
Xiao, J., Kannan, G., Jones-Brando, L., Brannock, C., Krasnova, I. N., Cadet, J. L., Pletnikov, M. and Yolken, R. H. (2012). Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience 206, 3948.
Yolken, R. H., Dickerson, F. B. and Fuller Torrey, E. (2009). Toxoplasma and schizophrenia. Parasite Immunology 31, 706715.
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Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
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