Impaired health status and increased incidence of diseases in Toxoplasma-seropositive subjects - An explorative cross-sectional study

Parasitology

Volumn 143, Issue 14, 2016, Pages 1974-1989

  Flegr, J ^a,b   Escudero, D Q ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (Czech Republic)

Author keywords

disease burden; neglected disease; neglected zoonosis; Parasite; public health; Toxoplasma gondii; toxoplasmosis

Indexed keywords

AGE DISTRIBUTION; ALTERNATIVE MEDICINE; ARTICLE; BRONCHITIS; COHORT ANALYSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; EXPLORATORY RESEARCH; FEMALE; HEALTH DISPARITY; HUMAN; HUMAN EXPERIMENT; INCIDENCE; INSOMNIA; LATENT TOXOPLASMOSIS; MALE; MENTAL DISEASE; MENTAL HEALTH; NORMAL HUMAN; PNEUMONIA; PREVALENCE; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; PUBLIC HEALTH PROBLEM; SEROPREVALENCE; SEX DIFFERENCE; SEXUAL BEHAVIOR; TOXOPLASMA; TOXOPLASMOSIS; UROGENITAL TRACT INFECTION; ADULT; ANIMAL; BLOOD; CASE CONTROL STUDY; COMPLICATION; HEALTH STATUS; IMMUNOLOGY; ISOLATION AND PURIFICATION; PARASITE LOAD; PARASITOLOGY; PATHOGENICITY; PUBLIC HEALTH; RISK FACTOR; SEROEPIDEMIOLOGY; TRANSMISSION; YOUNG ADULT;

PROTOZOON ANTIBODY;

ADULT; ANIMALS; ANTIBODIES, PROTOZOAN; CASE-CONTROL STUDIES; COHORT STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; HEALTH STATUS; HUMANS; INCIDENCE; MALE; PARASITE LOAD; PUBLIC HEALTH; RISK FACTORS; SEROEPIDEMIOLOGIC STUDIES; TOXOPLASMA; TOXOPLASMOSIS; YOUNG ADULT;

EID: 84990895440     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182016001785     Document Type: Article

References (79)

1. Addebbous, A., Adarmouch, L., Tali, A., Laboudi, M., Amine, M., Aajly, L., Rhajaoui, M., Chabaa, L. and Zougaghi, L. (2012). IgG anti-Toxoplasma antibodies among asymptomatic HIV-infected patients in Marrakesh-Morocco. Acta Tropica 123, 49-52.
2. Akanmu, A. S., Osunkalu, V. O., Ofomah, J. N. and Olowoselu, F. O. (2010). Pattern of demographic risk factors in the seroprevalence of anti-Toxoplasma gondii antibodies in HIV infected patients at the Lagos University Teaching Hospital. Nigerian Quarterly Journal of Hospital Medicine 20, 1-4.
3. 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. In Parasites & Vectors, Vol. 5. doi: 10. 1186/1756-3305-5-13.
4. Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289-300.
5. 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.
6. Bhadra, R., Cobb, D. A., Weiss, L. M. and Khan, I. A. (2013). Psychiatric disorders in Toxoplasma seropositive patients-CD8 connection. Schizophrenia Bulletin 39, 485-489.
7. Blomstrom, A., Karlsson, H., Wicks, S., Yang, S., Yolken, R. H. and Dalman, C. (2012). Maternal antibodies to infectious agents and risk for non-affective psychoses in the offspring-a matched case-control study. Schizophrenia Research 140, 25-30.
8. Coppens, I. (2006). Contribution of host lipids to Toxoplasma pathogenesis. Cell Microbiol 8, 1-9.
9. Flegr, J. (2010). Influence of latent toxoplasmosis on the phenotype of intermediate hosts. Folia Parasitologica 57, 81-87.
10. Flegr, J. (2013). How and why Toxoplasma makes us crazy. Trends in Parasitology 29, 156-163.
11. Flegr, J. (2013). Influence of latent Toxoplasma infection on human personality, physiology and morphology: pros and cons of the Toxoplasmahuman model in studying the manipulation hypothesis. Journal of Experimental Biology 216, 127-133.
12. Flegr, J. (2016). Could contamination of data with misclassified individuals increase the probability of false positive results of statistical tests?. Figshare. https: //dx. doi. org/10. 6084/m9. figshare. 3806553. v1.
13. Flegr, J. and Hodny, Z. (2016). Cat scratches, not bites, are associated with unipolar depression-cross-sectional study. Parasites & Vectors 9. doi: 10. 1186/s13071-015-1290-7.
14. Flegr, J. and Hrdý, I. (1994). Influence of chronic toxoplasmosis on some human personality factors. Folia Parasitologica 41, 122-126.
15. Flegr, J. and St?íž, I. (2011). Potential immunomodulatory effects of latent toxoplasmosis in humans. BMC Infectious Diseases 11, 274.
16. Flegr, J., Zitkova, S., Kodym, P. and Frynta, D. (1996). Induction of changes in human behaviour by the parasitic protozoan Toxoplasma gondii. Parasitology 113, 49-54.
17. Flegr, J., Havlí?ek, J., Kodym, P., Malý, M. and Šmahel, Z. (2002). Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study. BMC Infectious Diseases 2, art-11.
18. Flegr, J., Preiss, M., Klose, J., Havlí?ek, 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, 253-268.
19. Flegr, J., Lindová, J. and Kodym, P. (2008). Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology 135, 427-431.
20. Flegr, J., Klose, J., Novotná, M., Berenreitterová, M. and Havlí?ek, J. (2009). Increased incidence of traffic accidents in Toxoplasma-infected military drivers and protective effect RhD molecule revealed by a large-scale prospective cohort study. BMC Infectious Diseases 9, art. 72.
21. Flegr, J., Hampl, R., ?ernochová, D., Preiss, M., Bi?íkova, M., Sieger, L., P?íplatová, L., Ka?ková, S. and Klose, J. (2012). The relation of cortisol and sex hormone levels to results of psychological, performance, IQ and memory tests in military men and women. Neuroendocrinology Letters 33, 224-235.
22. Flegr, J., Prandota, J., Sovickova, M. and 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. doi: 10. 1371/journal. pone. 0090203.
23. 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.
24. Gale, S. D., Brown, B. L., Berrett, A., Erickson, L. D. and Hedges, D. W. (2014). Association between latent toxoplasmosis and major depression, generalised anxiety disorder and panic disorder in human adults. Folia Parasitologica 61, 285-292.
25. Gaskell, E. A., Smith, J. E., Pinney, J. W., Westhead, D. R. and McConkey, G. A. (2009). A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE 4, e4801.
26. Guthrie, K. A. and Sheppard, L. (2001). Overcoming biases and misconceptions in ecological studies. Journal of the Royal Statistical Society: Series A (Statistics in Society) 164, 141-154.
27. Havlí?ek, J., Gašová, Z., Smith, A. P., Zvára, K. and Flegr, J. (2001). Decrease of psychomotor performance in subjects with latent 'asymptomatic' toxoplasmosis. Parasitology 122, 515-520.
28. Hsu, P. C., Groer, M. and Beckie, T. (2014). New findings: depression, suicide, and Toxoplasma gondii infection. Journal of the American Association of Nurse Practitioners 26, 629-637.
29. Jones, J. L. and Holland, G. N. (2010). Annual burden of ocular toxoplasmosis in the US. American Journal of Tropical Medicine and Hygiene 82, 464-465.
30. Ka?ková, Š., Kodym, P. and Flegr, J. (2011). Direct evidence of Toxoplasma-induced changes in serum testosterone in mice. Experimental Parasitology 128, 181-183.
31. Kankova, S., Prochazkova, L., Flegr, J., Calda, P., Springer, D. and Potlukova, E. (2014). Effects of latent toxoplasmosis on autoimmune thyroid diseases in pregnancy. PLoS ONE 9. doi: 10. 1371/journal. pone. 0110878.
32. Kankova, S., Flegr, J. and Calda, P. (2015). The influence of latent toxoplasmosis on women's reproductive function: four cross-sectional studies. Folia Parasitologica 62, 041. doi: 10. 14411/fp. 2015. 041.
33. Ka?ková, Š., Flegr, J. and Calda, P. (2015). An elevated blood glucose level and increased incidence of gestational diabetes mellitus in pregnant women with latent toxoplasmosis. Folia Parasitologica 62, 1-6.
34. Kapoor, S. (2012). The close relationship between toxoplasmosis and kidney function. Revista do Instituto de Medicina Tropical de Sao Paulo 54, 318-318.
35. Koseoglu, E., Yazar, S. and Koc, I. (2009). Is Toxoplasma gondii a causal agent in migraine? American Journal of the Medical Sciences 338, 120-122.
36. Lambert, H., Dellacasa-Lindberg, I. and Barragan, A. (2011). Migratory responses of leukocytes infected with Toxoplasma gondii. Microbes and Infection 13, 96-102.
37. Lim, A., Kumar, V., Hari Dass, S. A. and Vyas, A. (2013). Toxoplasma gondii infection enhances testicular steroidogenesis in rats. Molecular Ecology 22, 102-110.
38. Lindová, J., Novotná, M., Havlí?ek, J., Jozífková, E., Skallová, A., Kolbeková, P., Hodný, Z., Kodym, P. and Flegr, J. (2006). Gender differences in behavioural changes induced by latent toxoplasmosis. International Journal for Parasitology 36, 1485-1492.
39. Lindová, J., Kub?na, A. A., Šturcová, A., K?ivohlavá, R., Novotná, M., Rubešová, A., Havlí?ek, J., Kodym, P. and Flegr, J. (2010). Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii-induced behavioural changes. Folia Parasitologica 57, 136-142.
40. Ling, V. J., Lester, D., Mortensen, P. B. and Postolache, T. T. (2011). Toxoplasma gondii seropositivity and completed suicide in 20 European countries. Biological Psychiatry 69, 500.
41. Markovitz, A. A., Simanek, A. M., Yolken, R. H., Galea, S., Koenen, K. C., Chen, S. and Aiello, A. E. (2015). Toxoplasma gondii and anxiety disorders in a community-based sample. Brain, Behavior, and Immunity 43, 192-197.
42. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. and Tauxe, R. V. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases 5, 607-625.
43. Montoya, J. G. and Liesenfeld, O. (2004). Toxoplasmosis. Lancet 363, 1965-1975.
44. Nagineni, C. N., Detrick, B. and Hooks, J. J. (2002). Transforming growth factor-beta expression in human retinal pigment epithelial cells is enhanced by Toxoplasma gondii: a possible role in the immunopathogenesis of retinochoroiditis. Clinical and Experimental Immunology 128, 372-378.
45. Nejad, M. R., Rostami, K., Cheraghipour, K., Mojarad, E. N., Volta, U., Al Dulaimi, D. and Zali, M. R. (2011). Celiac disease increases the risk of Toxoplasma gondii infection in a large cohort of pregnant women. American Journal of Gastroenterology 106, 548-549.
46. Ngoungou, E. B., Bhalla, D., Nzoghe, A., Darde, M.-L. and Preux, P.-M. (2015). Toxoplasmosis and epilepsy-systematic review and meta analysis. PLoS Neglected Tropical Diseases 9. doi: 10. 1371/journal. pntd. 0003525.
47. Palmer, B. S. (2007). Meta-analysis of three case controlled studies and an ecological study into the link between cryptogenic epilepsy and chronic toxoplasmosis infection. Seizure 16, 657-663.
48. Pappas, G., Roussos, N. and Falagas, M. E. (2009). Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. International Journal for Parasitology 39, 1385-1394.
49. Paspalaki, P. K., Mihailidou, E. P., Bitsori, M., Tsagkaraki, D. and Mantzouranis, E. (2001). Polyomyositis and myocarditis associated with acquired toxoplasmosis in an immunocompetent girl. BMC Musculoskeletal Disorders 2, 8.
50. Pearce, B. D., Kruszon-Moran, D. and Jones, J. L. (2012). The relationship between Toxoplasma gondii infection and mood disorders in the Third National Health and Nutrition Survey. Biological Psychiatry 72, 290-295.
51. Pedersen, M. G., Mortensen, P. B., Norgaard-Pedersen, B. and Postolache, T. T. (2012). Toxoplasma gondii infection and self-directed violence in mothers. Archives of General Psychiatry 69, 1123-1130.
52. Porter, S. B. and Sande, M. A. (1992). Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. New England Journal of Medicine 327, 1643-1648.
53. Prandota, J. (2009). The importance of Toxoplasma gondii infection in diseases presenting with headaches. Headaches and aseptic meningitis may be manifestations of the Jarisch-Herxheimer reaction. International Journal of Neuroscience 119, 2144-2182.
54. Prandota, J. (2010). Neuropathological changes and clinical features of autism spectrum disorder participants are similar to that reported in congenital and chronic cerebral toxoplasmosis in humans and mice. Research in Autism Spectrum Disorders 4, 103-118.
55. Prandota, J. (2012). Gastrointestinal tract abnormalities in autism, inflammatory bowel disease and many other clinical entities may be due to T. gondii infection. Open Access Scientific Reports 1, 256.
56. 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.
57. Radford, A., Williams, S. N., Kane, B. and Groer, M. (2012). Relationships of Toxoplasma antibody titers and dysphoric moods in female veterans. Brain Behavior and Immunity 26, S23.
58. Sanchis-Belenguer, R., Cuadrado-Mendez, L. and Ortiz Munoz, A. B. (1984). [Possible interactions between Toxoplasma gondii infection and the presence of carcinomas of female genitalia and the breast]. Revista Espanola de Oncologia 31, 247-255.
59. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., Jones, J. L. and Griffin, P. M. (2011). Foodborne illness acquired in the United States-major pathogens. Emerging Infectious Diseases 17, 7-15.
60. Shapira, Y., Agmon-Levin, N., Selmi, C., Petrikova, J., Barzilai, O., Ram, M., Bizzaro, N., Valentini, G., Matucci-Cerinic, M., Anaya, J.-M., Katz, B.-S. P. and Shoenfeld, Y. (2012). Prevalence of anti-Toxoplasma antibodies in patients with autoimmune diseases. Journal of Autoimmunity 39, 112-116.
61. Siegel, S. and Castellan, N. J. (1988). Nonparametric Statistics for the Behavioral Sciences, 2nd Edn. McGraw-Hill, New York.
62. Singh, S., Singh, N., Pandav, R., Pandav, C. S. and Karmarkar, M. G. (1994). Toxoplasma gondii infection & its association with iodine deficiency in a residential school in a tribal area of Maharashtra. Indian Journal of Medical Research 99, 27-31.
63. Skallová, A., Novotná, M., Kolbeková, P., Gašová, Z., Veselý, V. and Flegr, J. (2005). Decreased level of novelty seeking in blood donors infected with Toxoplasma. Neuroendocrinology Letters 26, 480-486.
64. Stommel, E. W., Seguin, R., Thadani, V. M., Schwartzman, J. D., Gilbert, K., Ryan, K. A., Tosteson, T. D. and Kasper, L. H. (2001). Cryptogenic epilepsy: an infectious etiology? Epilepsia 42, 436-438.
65. Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217-1258.
66. Tomairek, H. A., Saeid, M. S., Morsy, T. A. and Michael, S. A. (1982). Toxoplasma gondii as a cause of rheumatoid arthritis. Journal of the Egyptian Society of Parasitology 12, 17-23.
67. Toporovski, J., Romano, S., Hartmann, S., Benini, W. and Chieffi, P. P. (2012). Nephrotic syndrome associated with toxoplasmosis: Report of seven cases. Revista do Instituto de Medicina Tropical de Sao Paulo 54, 61-64.
68. Torrey, E. F. and Yolken, R. H. (2001). The schizophrenia-rheumatoid arthritis connection: infectious, immune, or both? Brain Behavior and Immunity 15, 401-410.
69. Torrey, E. F., Bartko, J. J., Lun, Z. R. and Yolken, R. H. (2007). Antibodies to Toxoplasma gondii in patients with schizophrenia: a metaanalysis. Schizophrenia Bulletin 33, 729-736.
70. Torrey, E. F., Bartko, J. J. and Yolken, R. H. (2012). Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophrenia Bulletin 38, 642-647.
71. Ustun, S., Aksoy, U., Dagci, H. and Ersoz, G. (2004). Incidence of toxoplasmosis in patients with cirrhosis. World Journal of Gastroenterology 10, 452-454.
72. Vaillant, V., de Valk, H., Baron, E., Ancelle, T., Colin, P., Delmas, M. C., Dufour, B., Pouillot, R., Le Strat, Y., Weinbreck, P., Jougla, E. and Desenclos, J. C. (2005). Foodborne infections in France. Foodborne Pathogens and Disease 2, 221-232.
73. van Velthuysen, M. L. and Florquin, S. (2000). Glomerulopathy associated with parasitic infections. Clinical Microbiology Reviews 13, 55-66.
74. Vethanyagam, A. and Bryceson, A. D. (1976). Acquired toxoplasmosis presenting as hepatitis. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 524-525.
75. Vos, G. H. (1987). Population studies showing cross-reactivity of Toxoplasma gondii antibodies with antibodies to malignant cervical tissue antigens. South African Medical Journal 71, 78-82.
76. Wakefield, J. and Salway, R. (2001). A statistical framework for ecological and aggregate studies. Journal of the Royal Statistical Society: Series A (Statistics in Society) 164, 119-137.
77. Webster, J. P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid. Rattus norvegicus Parasitology 109, 583-589.
78. Yagmur, F., Yazar, S., Temel, H. O. and Cavusoglu, M. (2010). May Toxoplasma gondii increase suicide attempt-preliminary results in Turkish subjects? Forensic Science International 199, 15-17.
79. Yazar, S., Gur, M., Ozdogru, I., Yaman, O., Oguzhan, A. and Sahin, I. (2006). Anti-Toxoplasma gondii antibodies in patients with chronic heart failure. Journal of Medical Microbiology 55, 89-92.