Loop-Mediated Isothermal Amplification (LAMP) Assay to Detect Toxoplasmosis in Schizophrenia Patients
-
Hadi MIRAHMADI
,
Raheleh HASANZADEH
,
Hamid MALEK RAEESI
,
Shirzad FALLAHI
,
Mahdi KHOSHSIMA SHAHRAKI
,
Alireza BADIRZADEH
Abstract
Background: Toxoplasma gondii (T. gondii) causes an important parasitic infection known as toxoplasmosis, which is a globally distributed important zoonosis. One of the major serious characteristics of T. gondii is its ability to manipulate the behavior of intermediate hosts. We performed a cross-sectional study to determine toxoplasmosis in schizophrenic patients, as one of the major neuropsychiatric disorders, using loop-mediated isothermal amplification (LAMP) technic by targeting parasite B1 gene.
Methods: Blood samples were taken from 118 schizophrenic patients hospitalized in tow hospitals including Baharan, Clinic of Psychiatric Ali-ibn-Abi-Talib Hospital (in Zahedan City), and Amir-al Momenin Psychiatric Hospital (in Zabol City), Sistan and Baluchestan Province, southeast Iran in 2016. They were analyzed using LAMP, and compared with the previous data of nested-PCR and serology.
Results: Out of the 118 schizophrenic individuals, 56 patients (47.4%) were found to be infected with T. gondii. The diagnosis of toxoplasmosis was confirmed in 41 patients (34.7%) via the nested-PCR. The seroprevalence of toxoplasmosis in schizophrenic patients was 55.9% (66/118).
Conclusion: We found a high efficiency of LAMP method in identifying toxoplasmosis and its high prevalence among schizophrenic patients. Our findings could provide viable offer implications for the prevention of schizophrenia.
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2. Yolken R, Dickerson F, Fuller Torrey E. Toxoplasma and schizophrenia. Parasite Immunol. 2009; 31(11):706-15.
3. Torrey EF, Bartko JJ, Lun Z-R, et al. Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr Bull. 2007; 33(3):729-36.
4. Torrey EF, Bartko JJ, Yolken RH. Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophr Bull. 2012; 38(3):642-7.
5. Ullmann LS, Gravinatti ML, Yamatogi RS, et al. Serosurvey of anti- Leptospira sp. and anti- Toxoplasma gondii antibodies in capybaras and collared and white-lipped peccaries. Revista da Sociedade Brasileira de Medicina Tropical. 2017; 50(2):248-50.
6. Mahmoudvand H, Sheibani V, Shojaee S, et al. Toxoplasma gondii infection potentiates cognitive impairments of Alzheimer's disease in the BALB/c mice. J Parasitol. 2016; 102(6): 629-635.
7. Alipour A, Shojaee S, Mohebali M, et al. Toxoplasma infection in schizophrenia patients: a comparative study with control group. Iran J Parasitol. 2011; 6(2): 31-37.
8. Rostami A, Seyyedtabaei SJ, Aghamolaie S, et al. Seroprevalence and risk factors associated with Toxoplasma gondii infection among rural communities in northern Iran. Rev Inst Med Trop Sao Paulo. 2016; 58(70).
9. Flegr J. Schizophrenia and Toxoplasma gondii: an undervalued association? Expert Rev Anti Infect Ther. 2015; 13(7):817-820.
10. Sugden K, Moffitt TE, Pinto L, et al. Is Toxoplasma gondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLoS One. 2016; 11(2):e0148435.
11. Karabulut N, Bilgiç S, Gürok MG, et al. Is there any role of latent toxoplasmosis in schizophrenia disease? Journal of the Chinese Medical Association. 2015; 78(9):533-7.
12. De Witte LD, Van Mierlo HC, Litjens M, et al. The association between antibodies to neurotropic pathogens and schizophrenia: a case-control study. npj Schizophrenia. 2015; 1:15041.
13. Abdollahian E, Shafiei R, Mokhber N, et al. Seroepidemiological study of Toxoplasma gondii infection among psychiatric patients in Mashhad, northeast of Iran. Iran J Parasitol. 2017; 12(1):117-122.
14. Khademvatan S, Khajeddin N, Izadi S, et al. Investigation of anti-Toxocara and anti-Toxoplasma antibodies in patients with schizophrenia disorder. Schizophr Res Treatment. 2014; 2014:230349.
15. Daryani A, Sarvi S, Aarabi M, et al. Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta Trop. 2014; 137:185-94.
16. Webster JP. The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull. 2007; 33(3):752-6.
17. Mahmoudvand H, Ziaali N, Aghaei I, et al. The possible association between Toxoplasma gondii infection and risk of anxiety and cognitive disorders in BALB/c mice. Pathog Glob Health. 2015; 109(8): 369-376.
18. Fallahi S, Seyyed Tabaei SJ, Pournia Y, et al. Comparison of loop-mediated isothermal amplification (LAMP) and nested-PCR assay targeting the RE and B1 gene for detection of Toxoplasma gondii in blood samples of children with leukaemia. Diagn Microbiol Infect Dis. 2014; 79(3):347-54.
19. Kumagai T, Furushima-Shimogawara R, Ohmae H, et al. Detection of early and single infections of Schistosoma japonicum in the intermediate host snail, Oncomelania hupensis, by PCR and loop-mediated isothermal amplification (LAMP) assay. Am J Trop Med Hyg. 2010; 83(3):542-8.
20. Ai L, Li C, Elsheikha H, et al. Rapid identification and differentiation of Fasciola hepatica and Fasciola gigantica by a loop-mediated isothermal amplification (LAMP) assay. Vet Parasitol. 2010; 174(3-4):228-33.
21. Ikadai H, Tanaka H, Shibahara N, et al. Molecular evidence of infections with Babesia gibsoni parasites in Japan and evaluation of the diagnostic potential of a loop-mediated isothermal amplification method. J Clin Microbiol. 2004; 42(6):2465-9.
22. Thekisoe OM, Inoue N, Kuboki N, et al. Evaluation of loop-mediated isothermal amplification (LAMP), PCR and parasitological tests for detection of Trypanosoma evansi in experimentally infected pigs. Vet Parasitol. 2005; 130(3-4):327-30.
23. Bakheit MA, Torra D, Palomino LA, et al. Sensitive and specific detection of Cryptosporidium species in PCR-negative samples by loop-mediated isothermal DNA amplification and confirmation of generated LAMP products by sequencing. Vet Parasitol. 2008; 158(1-2):11-22.
24. Rivera WL, Ong VA. Development of loop-mediated isothermal amplification for rapid detection of Entamoeba histolytica. Asian Pac J Trop Med. 2013; 6(6):457-61.
25. Paris DH, Imwong M, Faiz AM, et al. Loop-mediated isothermal PCR (LAMP) for the diagnosis of falciparum malaria. Am J Trop Med Hyg. 2007; 77(5):972-6.
26. Fallahi S, Mazar ZA, Ghasemian M, et al. Challenging loop—mediated isothermal amplification (LAMP) technique for molecular detection of Toxoplasma gondii. Asian Pac J Trop Med. 2015; 8(5):366-72.
27. First MB, Spitzer RL, Gibbon M, et al. The structured clinical interview for DSM-III-R personality disorders (SCID-II). Part II: Multi-site test-retest reliability study. J Pers Disord. 1995; 9(2):92-104.
28. Jafari Modrek M, Hasanzadeh R, Foroutan M, et al. Seroprevalence and molecular evaluation of Toxoplasma gondii in Schizophrenic patients hospitalized in Sistan and Baluchestan province, Southeast of Iran. Trop Biomed. 2018; 36(2): 422–429.
29. Keshavarz Valian H, Mirhendi H, Mohebali M, et al. Comparison of the RE-529 sequence and B1 gene for Toxoplasma gondii detection in blood samples of the at-risk seropositive cases using uracil DNA glycosylase supplemented loop-mediated isothermal amplification (UDG-LAMP) assay. Microb Pathog. 2020; 140):103938
30. Sotiriadou I, Karanis P. Evaluation of loop-mediated isothermal amplification for detection of Toxoplasma gondii in water samples and comparative findings by polymerase chain reaction and immunofluorescence test (IFT). Diagn Microbiol Infect Dis. 2008; 62(4):357-65.
31. Torrey EF, Yolken RH. Could schizophrenia be a viral zoonosis transmitted from house cats. Schizophr Bull. 1995; 21(2):167-71.
32. Zhou P, Chen Z, Li H-L, et al. Toxoplasma gondii infection in humans in China. Parasites & Vectors. 2011; 4(1):165.
33. Kheirandish F, Nazari H, Mahmoudvand H, et al. Possible Link Between Toxoplasma gondii Infection and Mood Disorders in Lorestan Province, Western Iran. Clin Infect Dis. 2016; 11(4):e36602.
34. Teimouri A, Mohtasebi S, Kazemirad E, et al. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. J Clin Microbiol. 2020; 58(9):e00505-20.
35. Mousavi P, Mirhendi H, Mohebali M, et al. Detection of Toxoplasma gondii in acute and chronic phases of infection in immunocompromised patients and pregnant women with real-time PCR assay using TaqMan fluorescent probe. Iran J Parasitol. 2018; 13(3): 373–381.
36. Modrek MJ, Mousavi M, Saravani R. Toxoplasma gondii seroprevalence among blood donors in Zahedan, southeastern Iran. International Journal of Infection. 2014; 1(2).
37. Meerburg BG, Kijlstra A. Changing climate—changing pathogens: Toxoplasma gondii in North-Western Europe. Parasitol Res. 2009; 105(1):17-24.
38. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000; 30(12-13):1217-58.
39. Kong Q-M, Lu S-H, Tong Q-B, et al. Loop-mediated isothermal amplification (LAMP): early detection of Toxoplasma gondii infection in mice. Parasit Vectors. 2012; 5:2.
40. Ghodrati M, Spotin A, Hazratian T, et al. Diagnostic Accuracy of Loop-mediated Isothermal Amplification Assay as a Field Molecular Tool for Rapid Mass Screening of Old World Leishmania Infections in Sand Flies and In Vitro Culture. Iran J Parasitol. 2017; 12(4):506-515.
2. Yolken R, Dickerson F, Fuller Torrey E. Toxoplasma and schizophrenia. Parasite Immunol. 2009; 31(11):706-15.
3. Torrey EF, Bartko JJ, Lun Z-R, et al. Antibodies to Toxoplasma gondii in patients with schizophrenia: a meta-analysis. Schizophr Bull. 2007; 33(3):729-36.
4. Torrey EF, Bartko JJ, Yolken RH. Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophr Bull. 2012; 38(3):642-7.
5. Ullmann LS, Gravinatti ML, Yamatogi RS, et al. Serosurvey of anti- Leptospira sp. and anti- Toxoplasma gondii antibodies in capybaras and collared and white-lipped peccaries. Revista da Sociedade Brasileira de Medicina Tropical. 2017; 50(2):248-50.
6. Mahmoudvand H, Sheibani V, Shojaee S, et al. Toxoplasma gondii infection potentiates cognitive impairments of Alzheimer's disease in the BALB/c mice. J Parasitol. 2016; 102(6): 629-635.
7. Alipour A, Shojaee S, Mohebali M, et al. Toxoplasma infection in schizophrenia patients: a comparative study with control group. Iran J Parasitol. 2011; 6(2): 31-37.
8. Rostami A, Seyyedtabaei SJ, Aghamolaie S, et al. Seroprevalence and risk factors associated with Toxoplasma gondii infection among rural communities in northern Iran. Rev Inst Med Trop Sao Paulo. 2016; 58(70).
9. Flegr J. Schizophrenia and Toxoplasma gondii: an undervalued association? Expert Rev Anti Infect Ther. 2015; 13(7):817-820.
10. Sugden K, Moffitt TE, Pinto L, et al. Is Toxoplasma gondii infection related to brain and behavior impairments in humans? Evidence from a population-representative birth cohort. PLoS One. 2016; 11(2):e0148435.
11. Karabulut N, Bilgiç S, Gürok MG, et al. Is there any role of latent toxoplasmosis in schizophrenia disease? Journal of the Chinese Medical Association. 2015; 78(9):533-7.
12. De Witte LD, Van Mierlo HC, Litjens M, et al. The association between antibodies to neurotropic pathogens and schizophrenia: a case-control study. npj Schizophrenia. 2015; 1:15041.
13. Abdollahian E, Shafiei R, Mokhber N, et al. Seroepidemiological study of Toxoplasma gondii infection among psychiatric patients in Mashhad, northeast of Iran. Iran J Parasitol. 2017; 12(1):117-122.
14. Khademvatan S, Khajeddin N, Izadi S, et al. Investigation of anti-Toxocara and anti-Toxoplasma antibodies in patients with schizophrenia disorder. Schizophr Res Treatment. 2014; 2014:230349.
15. Daryani A, Sarvi S, Aarabi M, et al. Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta Trop. 2014; 137:185-94.
16. Webster JP. The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull. 2007; 33(3):752-6.
17. Mahmoudvand H, Ziaali N, Aghaei I, et al. The possible association between Toxoplasma gondii infection and risk of anxiety and cognitive disorders in BALB/c mice. Pathog Glob Health. 2015; 109(8): 369-376.
18. Fallahi S, Seyyed Tabaei SJ, Pournia Y, et al. Comparison of loop-mediated isothermal amplification (LAMP) and nested-PCR assay targeting the RE and B1 gene for detection of Toxoplasma gondii in blood samples of children with leukaemia. Diagn Microbiol Infect Dis. 2014; 79(3):347-54.
19. Kumagai T, Furushima-Shimogawara R, Ohmae H, et al. Detection of early and single infections of Schistosoma japonicum in the intermediate host snail, Oncomelania hupensis, by PCR and loop-mediated isothermal amplification (LAMP) assay. Am J Trop Med Hyg. 2010; 83(3):542-8.
20. Ai L, Li C, Elsheikha H, et al. Rapid identification and differentiation of Fasciola hepatica and Fasciola gigantica by a loop-mediated isothermal amplification (LAMP) assay. Vet Parasitol. 2010; 174(3-4):228-33.
21. Ikadai H, Tanaka H, Shibahara N, et al. Molecular evidence of infections with Babesia gibsoni parasites in Japan and evaluation of the diagnostic potential of a loop-mediated isothermal amplification method. J Clin Microbiol. 2004; 42(6):2465-9.
22. Thekisoe OM, Inoue N, Kuboki N, et al. Evaluation of loop-mediated isothermal amplification (LAMP), PCR and parasitological tests for detection of Trypanosoma evansi in experimentally infected pigs. Vet Parasitol. 2005; 130(3-4):327-30.
23. Bakheit MA, Torra D, Palomino LA, et al. Sensitive and specific detection of Cryptosporidium species in PCR-negative samples by loop-mediated isothermal DNA amplification and confirmation of generated LAMP products by sequencing. Vet Parasitol. 2008; 158(1-2):11-22.
24. Rivera WL, Ong VA. Development of loop-mediated isothermal amplification for rapid detection of Entamoeba histolytica. Asian Pac J Trop Med. 2013; 6(6):457-61.
25. Paris DH, Imwong M, Faiz AM, et al. Loop-mediated isothermal PCR (LAMP) for the diagnosis of falciparum malaria. Am J Trop Med Hyg. 2007; 77(5):972-6.
26. Fallahi S, Mazar ZA, Ghasemian M, et al. Challenging loop—mediated isothermal amplification (LAMP) technique for molecular detection of Toxoplasma gondii. Asian Pac J Trop Med. 2015; 8(5):366-72.
27. First MB, Spitzer RL, Gibbon M, et al. The structured clinical interview for DSM-III-R personality disorders (SCID-II). Part II: Multi-site test-retest reliability study. J Pers Disord. 1995; 9(2):92-104.
28. Jafari Modrek M, Hasanzadeh R, Foroutan M, et al. Seroprevalence and molecular evaluation of Toxoplasma gondii in Schizophrenic patients hospitalized in Sistan and Baluchestan province, Southeast of Iran. Trop Biomed. 2018; 36(2): 422–429.
29. Keshavarz Valian H, Mirhendi H, Mohebali M, et al. Comparison of the RE-529 sequence and B1 gene for Toxoplasma gondii detection in blood samples of the at-risk seropositive cases using uracil DNA glycosylase supplemented loop-mediated isothermal amplification (UDG-LAMP) assay. Microb Pathog. 2020; 140):103938
30. Sotiriadou I, Karanis P. Evaluation of loop-mediated isothermal amplification for detection of Toxoplasma gondii in water samples and comparative findings by polymerase chain reaction and immunofluorescence test (IFT). Diagn Microbiol Infect Dis. 2008; 62(4):357-65.
31. Torrey EF, Yolken RH. Could schizophrenia be a viral zoonosis transmitted from house cats. Schizophr Bull. 1995; 21(2):167-71.
32. Zhou P, Chen Z, Li H-L, et al. Toxoplasma gondii infection in humans in China. Parasites & Vectors. 2011; 4(1):165.
33. Kheirandish F, Nazari H, Mahmoudvand H, et al. Possible Link Between Toxoplasma gondii Infection and Mood Disorders in Lorestan Province, Western Iran. Clin Infect Dis. 2016; 11(4):e36602.
34. Teimouri A, Mohtasebi S, Kazemirad E, et al. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in pregnancy. J Clin Microbiol. 2020; 58(9):e00505-20.
35. Mousavi P, Mirhendi H, Mohebali M, et al. Detection of Toxoplasma gondii in acute and chronic phases of infection in immunocompromised patients and pregnant women with real-time PCR assay using TaqMan fluorescent probe. Iran J Parasitol. 2018; 13(3): 373–381.
36. Modrek MJ, Mousavi M, Saravani R. Toxoplasma gondii seroprevalence among blood donors in Zahedan, southeastern Iran. International Journal of Infection. 2014; 1(2).
37. Meerburg BG, Kijlstra A. Changing climate—changing pathogens: Toxoplasma gondii in North-Western Europe. Parasitol Res. 2009; 105(1):17-24.
38. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000; 30(12-13):1217-58.
39. Kong Q-M, Lu S-H, Tong Q-B, et al. Loop-mediated isothermal amplification (LAMP): early detection of Toxoplasma gondii infection in mice. Parasit Vectors. 2012; 5:2.
40. Ghodrati M, Spotin A, Hazratian T, et al. Diagnostic Accuracy of Loop-mediated Isothermal Amplification Assay as a Field Molecular Tool for Rapid Mass Screening of Old World Leishmania Infections in Sand Flies and In Vitro Culture. Iran J Parasitol. 2017; 12(4):506-515.
| Files | ||
| Issue | Vol 15 No 3 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v15i3.4193 | |
| Keywords | ||
| Loop-mediated isother-mal amplification (LAMP) Toxoplasma gondii Toxoplasmosis Schizophrenia | ||
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How to Cite
1.
MIRAHMADI H, HASANZADEH R, MALEK RAEESI H, FALLAHI S, KHOSHSIMA SHAHRAKI M, BADIRZADEH A. Loop-Mediated Isothermal Amplification (LAMP) Assay to Detect Toxoplasmosis in Schizophrenia Patients. Iran J Parasitol. 2020;15(3):299-306.
