Schizophrenia Research and Treatment

Schizophrenia Research and Treatment / 2014 / Article

Research Article | Open Access

Volume 2014 |Article ID 230349 | 7 pages | https://doi.org/10.1155/2014/230349

Investigation of Anti-Toxocara and Anti-Toxoplasma Antibodies in Patients with Schizophrenia Disorder

Academic Editor: David C. Henderson
Received31 Dec 2013
Revised05 Mar 2014
Accepted20 Mar 2014
Published16 Apr 2014

Abstract

Objective. The aim of the present study was to examine the relationship between Toxoplasma gondii and Toxocara spp. infections in patients with schizophrenia disorder. Method. A total of 100 patients with schizophrenia disorder and 95 healthy individuals participated in the study. Participants were tested for the presence of anti-T. gondii and anti-Toxocara spp. antibodies by ELISA and Western blotting. Data were analyzed using Chi-square test and Fisher9s exact test. Results. There were no differences in T. gondii IgG seroprevalence between patients with schizophrenia and healthy individuals (), but there were differences in seroprevalence between males and females with schizophrenia (). In contrast, Toxocara spp. IgG seroprevalence was greater in patients with schizophrenia disorder than in healthy individuals (), but there were no differences in seroprevalence between men and women with schizophrenia (). Finally, there were no differences in seroprevalence of T. gondii or Toxocara spp. IgG among different subtypes of schizophrenia, various age groups, residential area, or clinical course of treatment (). Conclusion. The present study suggests that patients with schizophrenia disorder are at elevated risk of Toxocara spp. infection. Moreover, contamination with T. gondii is a risk factor for schizophrenia in women.

1. Introduction

Schizophrenia is a severe, disabling mental disorder with a devastating impact on patients, their family, and society [1]. Schizophrenia is a heterogeneous disorder characterized by a range of clinical features such as positive and negative symptoms [2], including a reduction in patients’ health-related quality of life [3]. The prevalence of schizophrenia has been reported to be 1% of the adult population [4], developing in late adolescence or early adulthood, and most patients suffer from the disease throughout their lifetime [1].

Toxocariasis is a helminthozoonosis, caused by the Ascaridida nematodes, Toxocara canis and Toxocara cati [5]. Dogs and cats are the definitive hosts of T. canis and T. cati, respectively, although other mammals, such as humans and rodents, can be infected [6]. Humans are infected by ingestion of infectious eggs [6], often as a result of direct contact with pets or consumption of contaminated vegetables or undercooked meat [7]. Toxocara infection is also often transmitted by contact with the soil. Young children, people who live in rural areas, and people with soil-related occupation are at increased risk for toxocariasis [810]. The presence of Toxocara spp. larvae in the central nervous system may cause some neurological and psychiatric disorders including schizophrenia. Kaplan et al. [11] found more seroprevalence of Toxocara spp. infection in patients with schizophrenia than in healthy individuals (45.9% versus 2%). Further, in the study conducted by El-Sayed and Ismail [12], toxocariasis was detected in 23.3% of patients with schizophrenia disorder compared with that in 2.2% of healthy controls. In another study by Alvarado-Esquivel [13], 4.7% of psychiatric inpatients were positive for anti-Toxocara IgG antibodies compared with 1.1% of healthy controls. The difference was statistically significant.

Another parasite that is thought to be associated with schizophrenia is Toxoplasma gondii. Toxoplasmosis is one of the most common parasitic infections in human and other warm-blooded vertebrates including birds, livestock, and marine mammals [14, 15]. Humans usually become infected by consumption of undercooked meat, unwashed or poorly washed vegetables, or contaminated drinking water [16]. After a short phase of acute toxoplasmosis, the infection becomes latent and becomes encysted in the central nervous system and in muscle tissues, potentially for the life of the infected host [17, 18]. The parasite has the ability to alter the behavior of the host to increase transmission [19]. Some studies have found changes in infected individuals’ personality characteristics [2024].

There is much evidence to suggest that schizophrenia disorder is associated with toxoplasmosis [2532]. Daryani et al. [33] and Hamidinejat et al. [34] from Iran also observed that higher titers of T. gondii IgG antibody was positively correlated with schizophrenia [3335]. Some results however challenge the plausibility of this association [36, 37]. Because of these controversial findings and little knowledge about the prevalence of Toxocara spp. infection in patients with schizophrenia, the present study aimed to determine the seroprevalence of Toxocara spp. and Toxoplasma infections in patients with schizophrenia disorder and to compare it with healthy controls in Ahvaz, Southwest Iran.

2. Methods

Research was conducted over a period of 12 months from 2012 to 2013. A total of 100 patients diagnosed as having schizophrenia disorder and 95 matched healthy controls participated in the study. The patients had been admitted into Golestan hospital affiliated to Jundishapur University of Medical Sciences in Ahvaz, Iran. The diagnosis of schizophrenia disorder was performed by two psychiatrists following the DSM-IV-TR criteria. The control group consisted of blood donors who were tested at the laboratory in Jundishapur University of Medical Sciences. The controls were assessed by both a clinical psychologist and a psychiatrist and had no history of schizophrenia disorder. Neither of the 2 groups were immunodeficient nor were any other major psychiatric disorders or neurological diseases presentable.

To participate, subjects had to agree to comply with the requirements of study, and after describing the procedures and purposes of the study, written informed consents were obtained. The hospital’s institutional review board approved all procedures.

A 5 mL blood sample was taken from each subject for serological analysis. Each subject was also asked to complete a questionnaire to obtain demographic data about ethnicity, gender, age, level of education obtained, marital status, and employment.

2.1. Serological Tests

Sera were separated by sample centrifugation at 3000 rpm for 5 min and then kept at −20°C until analysis. Anti-Toxoplasma antibodies (IgG and IgM) concentrations were measured by enzyme-linked immunosorbent assay (ELISA) (IgG and IgM: Trinity Biotech Captia, USA). In addition, all sera were examined by Toxocara IgG-ELISA test (IBL, International Gmbh, Hamburg, Germany) and Toxocara Western blot test (LDBIO Diagnostics, Lyon, France) for confirmation.

2.2. Statistical Analysis

Data were analyzed using Chi-square test, Fisher’s exact test, and Student’s -test. Odds ratios (OR) with 95% confidence intervals (CI) were also determined. was considered significant. Statistical analyses were carried out using SPSS v16 software.

3. Results

Demographic characteristics (sex, residence, marital status, level of education obtained, ethnicity, and age) of both patients and healthy controls are detailed in Table 1. Patient and control group seroprevalence for both T. gondii and Toxocara was evaluated. Anti-Toxplasma antibodies were detected in 34% of patients with schizophrenia disorder and 47.39% of healthy individuals () (Table 2). Anti-Toxoplasma IgM antibodies were positive in 4 patients and 2 healthy individuals ().


FeatureFrequency
Patients’ groupControl groupTotal

T.  gondii
 Positive34 (34%)45 (47.36%)79 (40.51%)
 Negative66 (66%)50 (52.63%)116 (59.48%)
Toxocara
 Positive14 (14%)4 (4.39%)18 (9.23%)
 Negative86 (86%)91 (95.78%)177 (90.76%)
Sex
 Female35 (35%)43 (45.74%)78 (40.20%)
 Male65 (65%)51 (54.25%)116 (59.79%)
Residence
 Urban76 (76%)89 (93.98%)165 (84.61%)
 Rural24 (24%)6 (6.31%)30 (15.38%)
Marital status
 Single64 (64%)77 (81.05%)141 (72.30%)
 Married25 (25%)18 (18.94%)43 (22.05%)
 Divorced/widowed11 (11%)0 (0)11 (5.64%)
Level of education
 Grade school 74 (74%)0 (0)74 (37.94%)
 12 years/high school18 (18%)9 (9.47%)27 (13.84%)
 University degree8 (8%)86 (90.52%)94 (48.20%)
Ethnicity
 Fars46 (48.42%)15 (17.85%)61 (34.07%)
 Arab15 (15.78%)33 (39.28%)48 (26.81%)
 Lor19 (20%)34 (40.47%)53 (29.60%)
 Others15 (15.78%)2 (2.38%)17 (9.49%)
Age (years)
 <200 (0)4 (4.21%)4 (2.05%)
 20–2932 (32%)83 (87.36%)115 (58.97%)
 30–3934 (34%)7 (7.36%)41 (21.02%)
 40–4923 (23%)0 (0)23 (11.79%)
 >5011 (11%)1 (1.05%)12 (6.15%)


Patients’ groupHealthySigORCI95
(%) (%)

Toxoplasma gondii 34/100 (34%)45/95 (47.36%)0.080.570.32–1.02
Toxocara 14/100 (14%)4/95 (4.3%)0.020.270.08–0.8

Seroprevalence of anti-Toxocara IgG were higher in schizophrenia patients (14%) than in healthy controls (4.3%) (; Table 2). Western blot analysis confirmed Toxocara spp. infection, with low molecular weight bands (24–35 kDa) that are specific for Toxocara IgG present from all positive sera.

With respect to schizophrenia subtypes, anti-T. gondii antibodies were present in 35.82% (24 of 67) of patients with paranoid type of schizophrenia disorder, 42.85% (3 of 7) of patients with catatonic type, 33.3% (6 of 18) of patients with undifferentiated type, and 33.3% (1 of 3) of patients with residual type. None of the patients with disorganized type were seropositive. The difference in infection rate among the subtypes was not statistically significant (, Table 3). Anti-Toxocara antibodies were detected in 1.56% (10 of 64) of patients with paranoid type of schizophrenia disorder, 14.28% (1 of 7) of patients with catatonic type, 11.11% (2 of 18) of patients with undifferentiated type, and 20% (1 of 5) patients with disorganized type. None of the patients with residual type were seropositive. The difference in infection rate among the subtypes was not statistically significant (, Table 3). Serological analyses also confirmed that there were no significant increases in anti-Toxocara and anti-Toxocara antibody levels in patients with first-episode Schizophrenia disorder compared with those in patients with recurrent episodes (, Table 4).


Subtypes of schizophreniaT. gondii
(%)
valueToxocara
(%)
value

Paranoid type24/67 (35.82%) 0.910/64 (1.56%) 0.5
Catatonic type3/7 (42.85%)1/7 (14.28%)
Residual type1/3 (33.3%)0/3 (0)
Undifferentiated type6/18 (33.3%)2/18 (11.11%)
Disorganized type 0/5 (0%)1/5 (20%)


Clinical course (%) valueORCI95

Toxoplasma gondii First episode13/30 (43.33%)0.12.080.84–5.12
Recurrent episodes18/67 (26.86%)
Toxocara First episode8/30 (26.66%)0.060.220.06–0.75
Recurrent episodes5/30 (16.66%)

The seroprevalence of anti-T. gondii IgG antibodies in male and female patients with schizophrenia disorder was 24.61% and 51.42%, respectively, (, Table 5). Anti-Toxocara antibodies were detected in 51.42% of females and 17.14% of males with schizophrenia disorder (nonsignificant). The seroprevalence of T. gondii infection in patients living in urban and rural areas was 21.05% and 16.66%, respectively, (nonsignificant, ). Seroprevalence of Toxocara also was not different between patients living in urban and rural areas (Table 6).


Patients’ group
(%)SigORCI
MaleFemale

Toxoplasma  gondii 16/65 (24.61%)18/35 (51.42%)0.0090.30.12–0.73
Toxocara8/65 (12.30%)6/35 (17.14%)0.51.470.46–4.65


Patients' group
(%)SigORCI
UrbanRural

Toxoplasma  gondii 16/76 (21.05%) 4/24 (16.66%) 0.7 1.36 0.39–4.7
Toxocara 6/76 (7.89%)3/24 (12.5%) 0.3 1.7 0.37–7.6

The participants were divided into 5 groups based on their age (20, 20–29, 30–39, 40–49, and 50 years). The seroprevalence of T. gondii infection in the five age groups were 0%, 32.25%, 40%, 26.08%, and 36.36%, respectively, in patients; in healthy individuals the seroprevalence was 0%, 44.57%, 71.42%, 0%, and 100%, respectively, (nonsignificant between or within age subgroups, , Table 7). For Toxocara seroprevalence, there were no differences between or within age subgroups (, Table 8). Anti-Toxocara antibodies were significantly more prevalent in men with schizophrenia disorder (12.30%) than in healthy men (1.92%) (), but there was no difference in women ().


Patients’ groupHealthySigORCI95
(%) (%)

Age (years)
 <200 (0%)0/4 (0%)
 20–2910/32 (32.25%)37/83 (44.57%)0.12.90.68–12.51
 30–3914/34 (41.17%)5/7 (71.42%)0.10.20.04–1.5
 40–496/23 (26.08%)0/0 (0%)
 >504/11 (36.36%)1/1 (100%)0.40.30.1–0.7


Patients’ groupHealthySigORCI95
(%) (%)

Age (years)
 <200 (0%)0 (0%)
 20–294/32 (12.5%)3/83 (4.81%)0.12.90.68–12.5
 30–396/34 (17.14%)1/7 (14.28%)0.61.20.12–12.2
 40–492/23 (8.69%)0/0 (0%)
 >502/11 (18.18%)0/1 (0%)0.80.810.61–1.08

4. Discussion

The present study was conducted to investigate associations between schizophrenia disorder and parasitic infections, toxocariasis and toxoplasmosis. Because of poor hygiene, the prevalence of Toxocara spp. is higher in most localities of Iran than any elsewhere in the world. Sharif et al. in northern Iran, Arbabi and Hooshyar in central Iran, Sadjjadi et al. in southern Iran, and Khademvatan et al. in Southwest Iran reported 44%, 13.3%, 52.8%, and 45%, respectively, [6, 3840]. With prevalence of approximately 50% in Iran, toxoplasmosis continues to be a public health problem [41]. The present study is the first to report toxocariasis in patients with schizophrenia in the Iranian population. The association between Toxoplasma gondii and schizophrenia also has received little attention in Iran.

The results of the present study show that there were significant differences between patients with schizophrenia disorder and healthy controls in seropositivity of Toxocara. We replicate the findings of the study conducted by Kaplan et al. [11] and El-Sayed and Ismail [12] that found that Toxocara spp. infection is related to schizophrenia disorder. Similarly, Alvarado-Esquivel [13] also reported that Toxocara infection is more frequent in patients with schizophrenia.

These results may be related to the fact that patients with schizophrenia have inadequate hygiene and self-care skills, and they have a greater tendency to eat inappropriate things [12]. Considering the correlation between lifestyle and Toxocara infection, and that Toxocara spp. is common in areas with low hygiene [11], abnormal behaviors and poor personal hygiene observed in patients with schizophrenia expose them to toxocariasis.

We considered gender differences in seroprevalence of Toxocara spp. infection. Although anti-toxocariasis IgG antibodies were significantly more prevalent in men with schizophrenia than in healthy men, no difference was found in seroprevalence of Toxocara infection between patients and healthy women. This may be related to the role of gender in the experience of illness, treatment, and recovery of schizophrenia disorder. Women with schizophrenia disorder have better global outcomes than men [42]; hence, it is less probable that women with schizophrenia are exposed to toxocariasis.

In the present study, there were no differences in the prevalence of Toxoplasma IgG seropositivity between patients with schizophrenia and healthy subjects. The finding is consistent with the result of the study conducted by Saraei-Sahnesaraei et al. [36] and Xiao et al. [37]. However, these results are in contrast to intervention studies [43, 44] and some direct studies [2531, 34, 35] that support the link between toxoplasmosis and schizophrenia disorder.

The reason for the difference in these findings may relate to the various genotypes of T. gondii that vary in prevalence geographically [36] and have distinct neuropathogenic potential [34, 35]. It also may be due to the timing and route of infection, varying degrees of pathogenicity among infecting organisms, or heterogeneous etiology of schizophrenia disorder [45].

There are a number of challenges to these types of epidemiological studies, including the relative insensitivity of some serological assays [46], arbitrary cutoff selection, classification by percentile ranges, grouping results as low, intermediate, or high, and analyzing antibody levels as a continuous rather than dichotomous or categorical variable [27].

In addition, for the purpose of respecting patients’ rights, only those who are able and willing to complete the informed consent form are able to participate in the studies. Previous research suggests that clinical symptoms of infected schizophrenic patients are more severe than those of noninfected patients [47], therefore reducing the probability of incorporating infected schizophrenic patients into studies.

In terms of gender difference, we found differences between male and female patients with schizophrenia disorder (). Similar results, that is, higher seropositivity in schizophrenic women than in schizophrenic men, were also reported by Dickerson et al. [48].

The present finding is in contrast with the studies conducted by Alvarado-Esquivel et al. [49], Yuksel [50], and Xiao et al. [37], which demonstrated that seroprevalence of anti-T. gondii IgG is not different between men and women with schizophrenia disorder. On the other hand, Lindová et al. [51] reported higher seropositivity in male than in female schizophrenic patients.

Higher burdens in women may be explained on the basis of animal studies. Spleens of male mice produce higher level of interferon-gamma (IFN) in the early stages of Toxoplasma infection than those of female mice. High levels of IFN and tumor necrosis factor-alpha help male mice to respond to T. gondii infection more rapidly and to control the parasite multiplication [52].

Regarding the residential area, some previous studies found that the risks for Toxocara and Toxoplasma infections are higher in rural areas than in urban areas [50, 5355]. Our study failed to show any differences between residential areas in the prevalence of infections, consistent with some other reports [12, 37].

Finally we did not find any significant differences in prevalence of toxoplasmosis and toxocariasis infections across various age subgroups, subtypes of schizophrenia, or between patients with first-episode schizophrenia disorder and those with recurrent episode schizophrenia.

The screening for Toxocara spp. antibodies depends on ELISA and Western blotting, which are the most common methods for immunodiagnosis of toxocariasis. Western blotting is more sensitive and specific than other available tests for diagnosing toxocariasis, capable of detecting low levels of Toxocara antibodies [56].

5. Conclusion

In conclusion, our research suggests that patients with schizophrenia disorder are at an elevated risk for Toxocara spp. infection. Moreover, contamination with T. gondii should be considered as one of the risk factors for schizophrenia disorder in women.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgments

This study was funded by Grant no. OG-90120 from Health Research Institute, Infectious and Tropical Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences and approved by the Ethical Committee (no.: ETH-658). The authors appreciate the support of the staff of the Protozoology Laboratory at Ahvaz Jundishapur University of Medical Sciences.

References

  1. L. Medeiros-Ferreira, J. E. Obiols, J. Navarro-Pastor, and A. Zuniga-Lagares, “Metabolic syndrome and health-related quality of life in patients with schizophrenia,” Actas Españolas de Psiquiatría, vol. 41, no. 1, pp. 17–26, 2013. View at: Google Scholar
  2. L. Cortese, R. Bressan, D. Castle, and S. Mosolov, “Management of Schizophrenia: clinical experience with asenapine,” Journal of Psychopharmacology, vol. 27, no. 4, pp. 14–22, 2013. View at: Publisher Site | Google Scholar
  3. N. Grano, M. Karjalainen, EdlundV et al., “Health-related quality of life among adolescents: a comparison between subjects at risk for psychosis and other help seekers,” Early Intervention in Psychiatry, 2013. View at: Publisher Site | Google Scholar
  4. E. Prandovszky, E. Gaskell, H. Martin, J. P. Dubey, J. P. Webster, and G. A. McConkey, “The neurotropic parasite Toxoplasma gondii increases dopamine metabolism,” PLoS ONE, vol. 6, no. 9, Article ID e23866, 2011. View at: Publisher Site | Google Scholar
  5. P. Congdon and P. Lloyd, “Toxocara infection in the United States: the relevance of poverty, geography and demography as risk factors, and implications for estimating county prevalence,” International Journal of Public Health, vol. 56, no. 1, pp. 15–24, 2011. View at: Publisher Site | Google Scholar
  6. S. Khademvatan, F. Rahim, M. Tavalla, R. Abdizadeh, and M. Hashemitabar, “PCR-based molecular characterization of Toxocara spp. using feces of stray cats: a study from Southwest Iran,” PLoS ONE, vol. 8, no. 6, Article ID e65293, 2013. View at: Google Scholar
  7. E. Pinelli, T. Herremans, M. G. Harms, D. Hoek, and L. M. Kortbeek, “Toxocara and ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 30, no. 7, pp. 873–879, 2011. View at: Publisher Site | Google Scholar
  8. J. Gawor, A. Borecka, H. Zarnowska, M. Marczyńska, and S. Dobosz, “Environmental and personal risk factors for toxocariasis in children with diagnosed disease in urban and rural areas of central Poland,” Veterinary Parasitology, vol. 155, no. 3-4, pp. 217–222, 2008. View at: Publisher Site | Google Scholar
  9. G. Quattrocchi, A. Nicoletti, B. Marin, E. Bruno, M. Druet-Cabanac et al., “Toxocariasis and epilepsy: systematic review and meta-analysis,” PLoS Neglected Tropical Diseases, vol. 6, Article ID e1775, 2012. View at: Google Scholar
  10. H. Smith, C. Holland, M. Taylor, J.-F. Magnaval, P. Schantz, and R. Maizels, “How common is human toxocariasis? Towards standardizing our knowledge,” Trends in Parasitology, vol. 25, no. 4, pp. 182–188, 2009. View at: Publisher Site | Google Scholar
  11. M. Kaplan, A. Kalkan, S. Kuk, K. Demirdag, M. Ozden, and S. S. Kilic, “Toxocara seroprevalence in schizophrenic patients in Turkey,” Yonsei Medical Journal, vol. 49, no. 2, pp. 224–229, 2008. View at: Publisher Site | Google Scholar
  12. N. M. El-Sayed and K. A. Ismail, “Relationship between Toxocara canis infection and schizophrenia,” Rawal Medical Journal, vol. 37, no. 2, pp. 155–161, 2012. View at: Google Scholar
  13. C. Alvarado-Esquivel, “Toxocara infection in psychiatric inpatients: a case control Seroprevalence study,” PLoS ONE, vol. 8, no. 4, Article ID e62606, 2013. View at: Google Scholar
  14. Y. Suzuki, “Host resistance in the brain against Toxoplasma gondii,” Journal of Infectious Diseases, vol. 185, no. 1, pp. S58–S65, 2002. View at: Publisher Site | Google Scholar
  15. J. P. Dubey, “Toxoplasma gondii infections in chickens (Gallus domesticus): Prevalence, clinical disease, diagnosis and public health significance,” Zoonoses and Public Health, vol. 57, no. 1, pp. 60–73, 2010. View at: Publisher Site | Google Scholar
  16. D. C. Herrmann, N. Pantchev, G. Vrhovec et al., “Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany,” International Journal for Parasitology, vol. 40, no. 3, pp. 285–292, 2010. View at: Publisher Site | Google Scholar
  17. J. P. Dubey and J. L. Jones, “Toxoplasma gondii infection in humans and animals in the United States,” International Journal for Parasitology, vol. 38, no. 11, pp. 1257–1278, 2008. View at: Publisher Site | Google Scholar
  18. C. M. Miller, N. R. Boulter, R. J. Ikin, and N. C. Smith, “The immunobiology of the innate response to Toxoplasma gondii,” International Journal for Parasitology, vol. 39, no. 1, pp. 23–39, 2009. View at: Publisher Site | Google Scholar
  19. E. Kristina and M. A. Fittipaldi, “Toxoplasma gondii as an etiological agent of schizophrenia essay,” Presented in Partial Fulfillment of the Requirements of the Degree of Master of Arts at Hofstra University, 2008. View at: Google Scholar
  20. J. Flegr, Š. Zitkovä, P. Kodym, and D. Frynta, “Induction of changes in human behaviour by the parasitic protozoan Toxoplasma gondii,” Parasitology, vol. 113, no. 1, pp. 49–54, 1996. View at: Google Scholar
  21. J. Flegr and J. Havlíček, “Changes in the personality profile of young women with latent toxoplasmosis,” Folia Parasitologica, vol. 46, no. 1, pp. 22–28, 1999. View at: Google Scholar
  22. J. Flegr, P. Kodym, and V. Tolarová, “Correlation of duration of latent Toxoplasma gondii infection with personality changes in women,” Biological Psychology, vol. 53, no. 1, pp. 57–68, 2000. View at: Publisher Site | Google Scholar
  23. M. Novotná, J. Hanusova, J. Klose et al., “Probable neuroimmunological link between Toxoplasma and cytomegalovirus infections and personality changes in the human host,” BMC Infectious Diseases, vol. 5, article 54, 2005. View at: Publisher Site | Google Scholar
  24. S. Khademvatan, S. Izadi-Mazidi, N. Khajeddin, and J. Saki, “Effect of toxoplasmosis on personality profiles of Iranian men and women,” South African Journal of Science, vol. 109, no. 1-2, pp. 1–4, 2013. View at: Google Scholar
  25. S. S. Mahmoud and M. S. Hasan, “Seroprevalence of Toxoplasmosis gondii among Schizophrenic patients,” Yemen Journal For Medical Science, vol. 1, no. 3, pp. 1–7, 2009. View at: Google Scholar
  26. P. Yuksel, B. Kocazeybek, N. Alpay, C. Babur, and R. Bayer, “Establishing the role of toxoplasmosis in the ethiopathogenesis of Schizophrenia,” in Proceedings of the 13th International Congress on Infectious Disease Abstracts, 2008. View at: Google Scholar
  27. D. W. Niebuhr, A. M. Millikan, D. N. Cowan, R. Yolken, Y. Li, and N. S. Weber, “Selected infectious agents and risk of schizophrenia among U.S. military personnel,” The American Journal of Psychiatry, vol. 165, no. 1, pp. 99–106, 2008. View at: Publisher Site | Google Scholar
  28. D. Hinze-Selch, W. Däubener, L. Eggert, S. Erdag, R. Stoltenberg, and S. Wilms, “A controlled prospective study of Toxoplasma gondii infection in individuals with schizophrenia: beyond seroprevalence,” Schizophrenia Bulletin, vol. 33, pp. 782–788, 2007. View at: Google Scholar
  29. P. B. Mortensen, B. Nørgaard-Pedersen, B. L. Waltoft et al., “Toxoplasma gondii as a risk factor for early-onset schizophrenia: analysis of filter paper blood samples obtained at birth,” Biological Psychiatry, vol. 61, no. 5, pp. 688–693, 2007. View at: Publisher Site | Google Scholar
  30. Z. Cetinkaya, S. Yazar, O. Gecici, and M. N. Namli, “Anti-Toxoplasma gondii antibodies in patients with schizophrenia—preliminary findings in a Turkish sample,” Schizophrenia Bulletin, vol. 33, no. 3, pp. 789–791, 2007. View at: Publisher Site | Google Scholar
  31. A. S. Brown, C. A. Schaefer, C. P. Quesenberry Jr., L. Liu, V. P. Babulas, and E. S. Susser, “Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring,” The American Journal of Psychiatry, vol. 162, no. 4, pp. 767–773, 2005. View at: Publisher Site | Google Scholar
  32. J. Horacek, J. Flegr, J. Tintera et al., “Latent toxoplasmosis reduces gray matter density in schizophrenia but not in controls: voxel-based-morphometry (VBM) study,” The World Journal of Biological Psychiatry, vol. 13, pp. 501–509, 2012. View at: Publisher Site | Google Scholar
  33. A. Daryani, M. Sharif, S. H. Hosseini, S. A. Karimi, and S. Gholami, “Serological survey of Toxoplasma gondii in schizophrenia patients referred to Psychiatric Hospital, Sari City, Iran,” Tropical Biomedicine, vol. 27, no. 3, pp. 476–482, 2010. View at: Google Scholar
  34. H. Hamidinejat, M. Ghorbanpoor, H. Hosseini et al., “Toxoplasma gondii infection in first-episode and inpatient individuals with schizophrenia,” International Journal of Infectious Diseases, vol. 14, pp. e978–e981, 2010. View at: Publisher Site | Google Scholar
  35. M. Sharif, M. Nasrolahei, S. Ziapour et al., “Toxocara cati infections in stray cats in northern Iran,” Journal of Helminthology, vol. 81, pp. 63–66, 2007. View at: Google Scholar
  36. M. Saraei-Sahnesaraei, F. Shamloo, H. Jahani Hashemi, F. Khabbaz, and S. Alizadeh, “Relation between Toxoplasma gondii infections and Schizophrenia,” Iranian Journal of Psychiatry and Clinical Psychology, vol. 15, no. 1, pp. 3–9, 2009. View at: Google Scholar
  37. Y. Xiao, J. Yin, N. Jiang et al., “Seroepidemiology of human Toxoplasma gondii infection in China,” BMC Infectious Diseases, vol. 10, article 4, 2010. View at: Publisher Site | Google Scholar
  38. M. Sharif, M. Nasrolahei, S. P. Ziapour et al., “Toxocara cati infections in stray cats in northern Iran,” Journal of Helminthology, vol. 81, no. 1, pp. 63–66, 2007. View at: Publisher Site | Google Scholar
  39. M. Arbabi and H. Hooshyar, “Gastrointestinal parasites of stray cats in Kashan, Iran,” Tropical Biomedicine, vol. 26, no. 1, pp. 16–22, 2009. View at: Google Scholar
  40. S. M. Sadjjadi, A. Oryan, A. R. Jalai, and D. Mehrabani, “Prevalence and intensity of infestation with Toxocara cati in stray cats in Shiraz, Iran,” Veterinarski Arhiv, vol. 71, no. 3, pp. 149–157, 2001. View at: Google Scholar
  41. M. Assmar, A. Amirkhani, N. Piazak, A. Hovanesian, A. Kooloobandi, and R. Etessami, “Toxoplasmosis in Iran, results of a seroepidemiological investigation,” Bulletin de la Societe de Pathologie Exotique, vol. 90, no. 1, pp. 19–21, 1997. View at: Google Scholar
  42. M. Sajatovic, J. H. Jenkins, M. E. Strauss, Z. A. Butt, and E. Carpenter, “Gender identity and implications for recovery among men and women with schizophrenia,” Psychiatric Services, vol. 56, no. 1, pp. 96–98, 2005. View at: Publisher Site | Google Scholar
  43. J. P. Webster, P. H. L. Lamberton, C. A. Donnelly, and E. F. Torrey, “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,” Proceedings of the Royal Society B, vol. 273, no. 1589, pp. 1023–1030, 2006. View at: Publisher Site | Google Scholar
  44. L. Jones-Brando, E. F. Torrey, and R. Yolken, “Drugs used in the treatment of schizophrenia and bipolar disorder inhibit the replication of Toxoplasma gondii,” Schizophrenia Research, vol. 62, no. 3, pp. 237–244, 2003. View at: Publisher Site | Google Scholar
  45. R. H. Yolken, F. B. Dickerson, and E. Fuller Torrey, “Toxoplasma and schizophrenia,” Parasite Immunology, vol. 31, no. 11, pp. 706–715, 2009. View at: Publisher Site | Google Scholar
  46. E. F. Torrey, J. J. Bartko, Z.-R. Lun, and R. H. Yolken, “Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis,” Schizophrenia Bulletin, vol. 33, no. 3, pp. 729–736, 2007. View at: Publisher Site | Google Scholar
  47. J. Flegr, “How and why Toxoplasma makes us crazy,” Trends in Parasitology, vol. 29, no. 4, pp. 155–163, 2013. View at: Google Scholar
  48. F. Dickerson, J. Boronow, C. Stallings, A. Origoni, and R. Yolken, “Toxoplasma gondii in individuals with schizophrenia: association with clinical and demographic factors and with mortality,” Schizophrenia Bulletin, vol. 33, no. 3, pp. 737–740, 2007. View at: Publisher Site | Google Scholar
  49. C. Alvarado-Esquivel, A. Sifuentes-Alvarez, S. G. Narro-Duarte et al., “Seroepidemiology of Toxoplasma gondii infection in pregnant women in a public hospital in northern Mexico,” BMC Infectious Diseases, vol. 6, article e113, 2006. View at: Publisher Site | Google Scholar
  50. P. Yuksel, N. Alpay, C. Babur et al., “The role of latent toxoplasmosis in the aetiopathogenesis of schizophrenia—the risk factor or an indication of a contact with cat?” Folia Parasitologica, vol. 57, no. 2, pp. 121–128, 2010. View at: Google Scholar
  51. J. Lindová, M. Novotná, J. Havlíček et al., “Gender differences in behavioral changes induced by latent toxoplasmosis,” International Journal for Parasitology, vol. 36, no. 14, pp. 1485–1492, 2006. View at: Publisher Site | Google Scholar
  52. J. Prandota, “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, vol. 4, no. 2, pp. 103–118, 2010. View at: Publisher Site | Google Scholar
  53. N. Doǧan, E. C. Dinleyici, O. Bor, S. O. Töz, and Y. Ozbel, “Seroepidemiological survey for Toxocara canis infection in the northwestern part of Turkey,” Turkiye Parazitoloji Dergisi, vol. 31, no. 4, pp. 288–291, 2007. View at: Google Scholar
  54. A. Deutz, K. Fuchs, H. Auer, U. Kerbl, H. Aspöck, and J. Köfer, “Toxocara-infestations in Austria: a study on the risk of infection of farmers, slaughterhouse staff, hunters and veterinarians,” Parasitology Research, vol. 97, no. 5, pp. 390–394, 2005. View at: Publisher Site | Google Scholar
  55. G. Rubinsky-Elefant, C. E. Hirata, J. H. Yamamoto, and M. U. Ferreira, “Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms,” Annals of Tropical Medicine and Parasitology, vol. 104, no. 1, pp. 3–23, 2010. View at: Publisher Site | Google Scholar
  56. M. Zibaei, F. Firoozeh, P. Bahrami, and S. M. Sajjadi, “Investigation of anti-Toxocara antibodies in epileptic patients and comparison of two methods: ELISA and Western blotting,” Epilepsy Research and Treatment, vol. 2013, Article ID 156815, 5 pages, 2013. View at: Publisher Site | Google Scholar

Copyright © 2014 Shahram Khademvatan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

2203 Views | 878 Downloads | 13 Citations
 PDF  Download Citation  Citation
 Download other formatsMore
 Order printed copiesOrder

We are committed to sharing findings related to COVID-19 as quickly and safely as possible. Any author submitting a COVID-19 paper should notify us at help@hindawi.com to ensure their research is fast-tracked and made available on a preprint server as soon as possible. We will be providing unlimited waivers of publication charges for accepted articles related to COVID-19. Sign up here as a reviewer to help fast-track new submissions.