Association between Toxocara Spp. Exposure and Schizophrenia: A Case-Control Study
-
Keivan Sahebi
,
Pouriya Akbari
,
Fattaneh Mikaeili
,
Rasoul Alimi
,
Mohammad Saleh Bahreini
,
Aref Teimouri
Abstract
Background: Toxocariasis is a zoonotic disease caused by the larvae of Toxocara canis or Toxocara cati. Patients with schizophrenia may be at higher risk of infection, possibly due to their cognitive and personal self-care impairments. We aimed to assess the association between Toxocara spp. exposure and schizophrenia.
Methods: This case-control study was conducted on 109 patients with schizophrenia admitted to Ibn Sina Hospital, Shiraz, Iran, and 104 age- and gender-matched healthy controls from May to September 2021. A questionnaire was obtained and serum samples were tested for IgG antibodies to Toxocara excretory/secretory (TES) antigens using an enzyme-linked immunosorbent assay (ELISA).
Results: Anti-Toxocara IgG was detected in 12 schizophrenic patients and 10 control subjects, giving respective seroprevalences of 11.0% (95% confidence interval [95% CI]=5.8–18.4%) and 9.6% (95% CI=4.7–17.0%). Univariate logistic analyses estimated an odds ratio (OR) of 1.16 (95% CI=0.44–3.16); however, it was not statistically significant (P=0.915). Individuals with a history of eating unwashed vegetables or fruits (23.1%, 95% CI=9.0–43.6, crude odds ratio [COR]=3.21, 95% CI=1.13–9.13) and rural residency (19.5%, 95% CI=8.8–34.9, COR=2.74, 95% CI=1.06–7.05) had significantly higher rates of seropositivity using the univariate logistic analyses. After multivariate logistic analyses, the differences were not statistically significant.
Conclusion: The toxocariasis seroprevalence among schizophrenic and healthy participants was not significantly different (11% vs. 9.6%). Since the disease severity, onset, and cognitive sequelae are not the same among schizophrenic patients, clinically matched studies with larger samples are required to address the current inconsistency between the studies.
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2. Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16(2):265-72.
3. Ma G, Rostami A, Wang T, Hofmann A, Hotez PJ, Gasser RB. Global and regional seroprevalence estimates for human toxocariasis: A call for action. Adv Parasitol. 2020;109:275-90.
4. Rostami A, Riahi SM, Holland CV, et al. Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019;13(12):e0007809.
5. Fillaux J, Magnaval J-F. Laboratory diagnosis of human toxocariasis. Vet Parasitol. 2013;193(4):327-36.
6. Magnaval J-F, Fabre R, Maurieres P, Charlet J-P, De Larrard B. Application of the western blotting procedure for the immunodiagnosis of human toxocariasis. Parasitol Res. 1991;77:697-702.
7. Schantz PM, Glickman LT. Toxocaral visceral larva migrans. N Engl J Med. 1978;298(8):436-9.
8. Moreira GMSG, de Lima Telmo P, Mendonça M, et al. Human toxocariasis: current advances in diagnostics, treatment, and interventions. Trends Parasitol. 2014;30(9):456-64.
9. Azam D, Ukpai OM, Said A, Abd-Allah GA, Morgan ER. Temperature and the development and survival of infective Toxocara canis larvae. Parasitol Res. 2012;110:649-56.
10. Edition F. Diagnostic and statistical manual of mental disorders. Am Psychiatr Assoc. 2013; 21:591–643.
11. Murray CJ, Lopez AD, WHO. The global burden of disease: a comprehensive assessment of mortality and disability from diseases, injuries, and risk factors in 1990 and projected to 2020: summary. WHO; 1996.
12. Charlson FJ, Ferrari AJ, Santomauro DF, et al. Global epidemiology and burden of schizophrenia: findings from the global burden of disease study 2016. Schizophr Bull. 2018;44(6):1195-1203.
13. Alavi SS, Mohammadi MR, Hooshyari Z, et al. Epidemiology of Psychotic Disorders Based on Demographic Variables in Iranian Children and Adolescents. Iran J Psychiatry. 2021;16(1):1-2.
14. Arias I, Sorlozano A, Villegas E, et al. Infectious agents associated with schizophrenia: a meta-analysis. Schizophr Res. 2012;136(1-3):128-36.
15. Nicoletti A. Neurotoxocariasis. Adv Parasitol. 2020;109:219-231.
16. Huminer D, Symon K, Groskopf I, et al. Seroepidemiologic study of toxocariasis and strongyloidiasis in institutionalized mentally retarded adults. Am J Trop Med Hyg. 1992;46(3):278-81.
17. Alvarado-Esquivel C. Toxocara infection in psychiatric inpatients: a case control seroprevalence study. PLoS One. 2013;8(4):e62606.
18. Cong W, Zhang X-X, Zhou N, et al. Toxocara seroprevalence among clinically healthy individuals, pregnant women and psychiatric patients and associated risk factors in Shandong Province, Eastern China. PLoS Negl Trop Dis. 2014;8(8):e3082.
19. Di Fiore M, Virga A, Usticano V, Di Rosa S, Rini G. Antibodies against Toxocara canis in human serum from western Sicily. Boll Ist Sieroter Milan. 1989;68(1):93-6.
20. Kaplan M, Kalkan A, Kuk S, Demirdag K, Ozden M, Kilic SS. Toxocara seroprevalence in schizophrenic patients in Turkey. Yonsei Med J. 2008;49(2):224-9.
21. El-Sayed NM, Ismail KA. Relationship between Toxocara canis infection and schizophrenia. Rawal Med J. 2012;37(02):155-61.
22. Khademvatan S, Khajeddin N, Izadi S, Yousefi E. Investigation of anti-Toxocara and anti-Toxoplasma antibodies in patients with schizophrenia disorder. Schizophr Res Treatment. 2014;2014: 230349.
23. Teimouri A, Nassrullah OJ, Hedayati P, et al. Prevalence and predictors of Toxoplasma gondii infection in psychiatric inpatients in Fars Province, Southern Iran. Front Psychiatry. 2022;13:891603.
24. Regier DA, Kuhl EA, Kupfer DJ. The DSM‐5: Classification and criteria changes. World Psychiatry. 2013;12(2):92-8.
25. Zibaei M, Sadjjadi SM, Sarkari B, Uga S. Evaluation of Toxocara cati excretory–secretory larval antigens in serodiagnosis of human toxocariasis. J Clin Lab Anal. 2016;30(3):248-53.
26. Taghipour A, Habibpour H, Mirzapour A, Rostami A. Toxocara infection/exposure and the risk of schizophrenia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg. 2021;115(10):1114-1121.
27. Abdi J, Darabi M, Sayehmiri K. Epidemiological situation of toxocariasis in Iran: meta-analysis and systematic review. Pak J Biol Sci. 2012;15(22):1052-5.
28. Rezaiemanesh MR, Afzalaghaee M, Hamidi S, Eshaghzadeh A, Paydar M, Hejazi SH. Prevalence of toxocariasis and its related risk factors in humans, dogs and cats in northeastern Iran: a population-based study. Trans R Soc Trop Med Hyg. 2019;113(7):399-409.
29. Abbaszadeh Afshar MJ, Zahabiun F, Heydarian P, et al. A systematic review and meta-analysis of toxocariasis in Iran: is it time to take it seriously? Acta Parasitol. 2020;65:569-84.
30. Sadjjadi S, Khosravi M, Mehrabani D, Oryan A. Seroprevalence of Toxocara infection in school children in Shiraz, Southern Iran. J Trop Pediatr. 2000;46(6):327-30.
31. Erfani A, Pouryousef A, Arefkhah N, et al. Seroprevalence of toxocariasis and its related risk factors among municipal street sweepers in Shiraz District in Fars Province, southern Iran. Clin Epidemiol Glob Health. 2020;8(2):643-6.
32. Rostami A, Ebrahimi M, Mehravar S, Omrani VF, Fallahi S, Behniafar H. Contamination of commonly consumed raw vegetables with soil transmitted helminth eggs in Mazandaran province, northern Iran. Int J Food Microbiol. 2016;225:54-8.
33. Gabrielli S, Tasić-Otašević S, Ignjatović A, et al. Seroprevalence and risk factors for Toxocara canis infection in Serbia during 2015. Foodborne Pathog Dis. 2017;14(1):43-9.
34. Lötsch F, Obermüller M, Mischlinger J, et al. Seroprevalence of Toxocara spp. in a rural population in Central African Gabon. Parasitol Int. 2016;65(6 Pt A):632-4.
35. Espinoza YA, Huapaya PE, Roldán WH, et al. Seroprevalence of human toxocariasis in Andean communities from the Northeast of Lima, Peru. Rev Inst Med Trop Sao Paulo. 2010;52:31-6.
36. Silva MB, Amor AL, Santos LN, et al. Risk factors for Toxocara spp. seroprevalence and its association with atopy and asthma phenotypes in school-age children in a small town and semi-rural areas of Northeast Brazil. Acta Trop. 2017;174:158-64.
37. Won KY, Kruszon-Moran D, Schantz PM, Jones JL. National seroprevalence and risk factors for zoonotic Toxocara spp. infection. Am J Trop Med Hyg. 2008;79(4):552-7.
38. Gyang PV, Akinwale OP, Lee Y-L, et al. Seroprevalence, disease awareness, and risk factors for Toxocara canis infection among primary schoolchildren in Makoko, an urban slum community in Nigeria. Acta Trop. 2015;146:135-40.
39. Smith H, Noordin R. Diagnostic limitations and future trends in the serodiagnosis of human toxocariasis. In Toxocara: the enigmatic parasite. 2006; pp:89-112.
2. Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16(2):265-72.
3. Ma G, Rostami A, Wang T, Hofmann A, Hotez PJ, Gasser RB. Global and regional seroprevalence estimates for human toxocariasis: A call for action. Adv Parasitol. 2020;109:275-90.
4. Rostami A, Riahi SM, Holland CV, et al. Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019;13(12):e0007809.
5. Fillaux J, Magnaval J-F. Laboratory diagnosis of human toxocariasis. Vet Parasitol. 2013;193(4):327-36.
6. Magnaval J-F, Fabre R, Maurieres P, Charlet J-P, De Larrard B. Application of the western blotting procedure for the immunodiagnosis of human toxocariasis. Parasitol Res. 1991;77:697-702.
7. Schantz PM, Glickman LT. Toxocaral visceral larva migrans. N Engl J Med. 1978;298(8):436-9.
8. Moreira GMSG, de Lima Telmo P, Mendonça M, et al. Human toxocariasis: current advances in diagnostics, treatment, and interventions. Trends Parasitol. 2014;30(9):456-64.
9. Azam D, Ukpai OM, Said A, Abd-Allah GA, Morgan ER. Temperature and the development and survival of infective Toxocara canis larvae. Parasitol Res. 2012;110:649-56.
10. Edition F. Diagnostic and statistical manual of mental disorders. Am Psychiatr Assoc. 2013; 21:591–643.
11. Murray CJ, Lopez AD, WHO. The global burden of disease: a comprehensive assessment of mortality and disability from diseases, injuries, and risk factors in 1990 and projected to 2020: summary. WHO; 1996.
12. Charlson FJ, Ferrari AJ, Santomauro DF, et al. Global epidemiology and burden of schizophrenia: findings from the global burden of disease study 2016. Schizophr Bull. 2018;44(6):1195-1203.
13. Alavi SS, Mohammadi MR, Hooshyari Z, et al. Epidemiology of Psychotic Disorders Based on Demographic Variables in Iranian Children and Adolescents. Iran J Psychiatry. 2021;16(1):1-2.
14. Arias I, Sorlozano A, Villegas E, et al. Infectious agents associated with schizophrenia: a meta-analysis. Schizophr Res. 2012;136(1-3):128-36.
15. Nicoletti A. Neurotoxocariasis. Adv Parasitol. 2020;109:219-231.
16. Huminer D, Symon K, Groskopf I, et al. Seroepidemiologic study of toxocariasis and strongyloidiasis in institutionalized mentally retarded adults. Am J Trop Med Hyg. 1992;46(3):278-81.
17. Alvarado-Esquivel C. Toxocara infection in psychiatric inpatients: a case control seroprevalence study. PLoS One. 2013;8(4):e62606.
18. Cong W, Zhang X-X, Zhou N, et al. Toxocara seroprevalence among clinically healthy individuals, pregnant women and psychiatric patients and associated risk factors in Shandong Province, Eastern China. PLoS Negl Trop Dis. 2014;8(8):e3082.
19. Di Fiore M, Virga A, Usticano V, Di Rosa S, Rini G. Antibodies against Toxocara canis in human serum from western Sicily. Boll Ist Sieroter Milan. 1989;68(1):93-6.
20. Kaplan M, Kalkan A, Kuk S, Demirdag K, Ozden M, Kilic SS. Toxocara seroprevalence in schizophrenic patients in Turkey. Yonsei Med J. 2008;49(2):224-9.
21. El-Sayed NM, Ismail KA. Relationship between Toxocara canis infection and schizophrenia. Rawal Med J. 2012;37(02):155-61.
22. Khademvatan S, Khajeddin N, Izadi S, Yousefi E. Investigation of anti-Toxocara and anti-Toxoplasma antibodies in patients with schizophrenia disorder. Schizophr Res Treatment. 2014;2014: 230349.
23. Teimouri A, Nassrullah OJ, Hedayati P, et al. Prevalence and predictors of Toxoplasma gondii infection in psychiatric inpatients in Fars Province, Southern Iran. Front Psychiatry. 2022;13:891603.
24. Regier DA, Kuhl EA, Kupfer DJ. The DSM‐5: Classification and criteria changes. World Psychiatry. 2013;12(2):92-8.
25. Zibaei M, Sadjjadi SM, Sarkari B, Uga S. Evaluation of Toxocara cati excretory–secretory larval antigens in serodiagnosis of human toxocariasis. J Clin Lab Anal. 2016;30(3):248-53.
26. Taghipour A, Habibpour H, Mirzapour A, Rostami A. Toxocara infection/exposure and the risk of schizophrenia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg. 2021;115(10):1114-1121.
27. Abdi J, Darabi M, Sayehmiri K. Epidemiological situation of toxocariasis in Iran: meta-analysis and systematic review. Pak J Biol Sci. 2012;15(22):1052-5.
28. Rezaiemanesh MR, Afzalaghaee M, Hamidi S, Eshaghzadeh A, Paydar M, Hejazi SH. Prevalence of toxocariasis and its related risk factors in humans, dogs and cats in northeastern Iran: a population-based study. Trans R Soc Trop Med Hyg. 2019;113(7):399-409.
29. Abbaszadeh Afshar MJ, Zahabiun F, Heydarian P, et al. A systematic review and meta-analysis of toxocariasis in Iran: is it time to take it seriously? Acta Parasitol. 2020;65:569-84.
30. Sadjjadi S, Khosravi M, Mehrabani D, Oryan A. Seroprevalence of Toxocara infection in school children in Shiraz, Southern Iran. J Trop Pediatr. 2000;46(6):327-30.
31. Erfani A, Pouryousef A, Arefkhah N, et al. Seroprevalence of toxocariasis and its related risk factors among municipal street sweepers in Shiraz District in Fars Province, southern Iran. Clin Epidemiol Glob Health. 2020;8(2):643-6.
32. Rostami A, Ebrahimi M, Mehravar S, Omrani VF, Fallahi S, Behniafar H. Contamination of commonly consumed raw vegetables with soil transmitted helminth eggs in Mazandaran province, northern Iran. Int J Food Microbiol. 2016;225:54-8.
33. Gabrielli S, Tasić-Otašević S, Ignjatović A, et al. Seroprevalence and risk factors for Toxocara canis infection in Serbia during 2015. Foodborne Pathog Dis. 2017;14(1):43-9.
34. Lötsch F, Obermüller M, Mischlinger J, et al. Seroprevalence of Toxocara spp. in a rural population in Central African Gabon. Parasitol Int. 2016;65(6 Pt A):632-4.
35. Espinoza YA, Huapaya PE, Roldán WH, et al. Seroprevalence of human toxocariasis in Andean communities from the Northeast of Lima, Peru. Rev Inst Med Trop Sao Paulo. 2010;52:31-6.
36. Silva MB, Amor AL, Santos LN, et al. Risk factors for Toxocara spp. seroprevalence and its association with atopy and asthma phenotypes in school-age children in a small town and semi-rural areas of Northeast Brazil. Acta Trop. 2017;174:158-64.
37. Won KY, Kruszon-Moran D, Schantz PM, Jones JL. National seroprevalence and risk factors for zoonotic Toxocara spp. infection. Am J Trop Med Hyg. 2008;79(4):552-7.
38. Gyang PV, Akinwale OP, Lee Y-L, et al. Seroprevalence, disease awareness, and risk factors for Toxocara canis infection among primary schoolchildren in Makoko, an urban slum community in Nigeria. Acta Trop. 2015;146:135-40.
39. Smith H, Noordin R. Diagnostic limitations and future trends in the serodiagnosis of human toxocariasis. In Toxocara: the enigmatic parasite. 2006; pp:89-112.
| Files | ||
| Issue | Vol 19 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i2.15857 | |
| Keywords | ||
| Case-control study Epidemiology Schizophrenia Toxocariasis Iran | ||
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How to Cite
1.
Sahebi K, Akbari P, Mikaeili F, Alimi R, Bahreini MS, Teimouri A. Association between Toxocara Spp. Exposure and Schizophrenia: A Case-Control Study. Iran J Parasitol. 2024;19(2):214-223.
