Review Article

Toxoplasma gondii Infection in Immunocompromised Patients in Iran (2013-2022): A Systematic Review and Meta-Analysis


Background: Toxoplasma gondii infection (toxoplasmosis) has the potential to cause a serious disease in immunocompromised patients and can be fatal in this population. We conducted a systematic review and meta-analysis to assess comprehensively the pooled seroprevalence of toxoplasmosis among immunocompromised patients including HIV/AIDS patients, cancer patients, and transplant recipients in Iran.

Methods: PubMed, Web of Science, Scopus, Embase, and Google Scholar databases (international) and Scientific Information Database (SID), Magiran, IranMedex, and IranDoc databases (national) were systematically searched for all reports that possibly contained data for T. gondii prevalence in different immunocompromised populations in Iran between 2013 and 2022.

Results: Overall, IgG seroprevalence rate of toxoplasmosis in Iranian immunocompromised patients was 45.1% (95% confidence interval (CI), 37.4–52.9). IgG seroprevalence rate of toxoplasmosis in 12 studies that included 2279 cancer patients, 19 studies that included 2565 HIV/AIDS patients and in 3 studies that included 200 transplant recipients was 43.6% (95% CI, 30.2–57.0), 45.9% (95% CI, 34.8–57.1) and 45.8% (95% CI, 32.5–59.0), respectively. Moreover, IgM seroprevalence rate in the 26 studies was 2.6% (95% CI, 1.4–3.7).

Conclusion: Our findings represent a high seroprevalence rate of Toxoplasma IgG among immunocompromised patients. Health improvement and education toward prevention of toxoplasmosis is of great importance for these susceptible populations.

1. Dubey JP. Toxoplasmosis of animals and humans, 2nd ed. CRC Press LLC, Boca Raton, FL. 2010.
2. Dubey J. History of the discovery of the life cycle of Toxoplasma gondii. Int J Parasitol. 2009;39:877-882.
3. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000;30:1217–1258.
4. Hill D, Dubey J. Toxoplasma gondii: trans-mission, diagnosis and prevention. Clin Microbiol Infect. 2002;8:634-640.
5. Shojaee S, Teimouri A, Keshavarz H, et al. The relation of secondary sex ratio and miscarriage history with Toxoplasma gondii infection. BMC Infect Dis. (2018) 18:307.
6. Teimouri A, Mohtasebi S, Kazemirad E, Keshavarz H. Role of Toxoplasma gondii IgG avidity testing in discriminating between acute and chronic toxoplasmosis in preg-nancy. J Clin Microbiol. (2020) 58:e00505-20.
7. Montoya JG, Liesenfeld O. Toxoplasmo-sis. Lancet. 2004;363:1965–76.
8. Hill DE, Chirukandoth S, Dubey JP. Biol-ogy and epidemiology of Toxoplasma gondii in man and animals. Anim Health Res Rev. 2005;6:41-61.
9. Mousavi P, Mirhendi H, Mohebali M, et al. Detection of Toxoplasma gondii in acute and chronic phases of infection in immuno-compromised patients and pregnant women with real-time PCR assay using TaqMan fluorescent probe. Iran J Parasi-tol. 2018; 13(3): 373–381.
10. Pappas G, Roussos N, Falagas, ME. Tox-oplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and impli-cations for pregnancy and congenital tox-oplasmosis. Int J Parasitol. 2009; 39:1385-1394.
11. Daryani A, Sarvi S, Aarabi M, et al. Sero-prevalence of Toxoplasma gondii in the Irani-an general population: a systematic review and meta-analysis. Acta Trop. 2014;137:185-194.
12. Foroutan M, Dalvand S, Daryani A, et al. Rolling up the pieces of a puzzle: a system-atic review and meta-analysis of the preva-lence of toxoplasmosis in Iran. Alexandria J Med. 2018;54:189-196.
13. Lewis JM, Clifford S, Nsutebu E. Toxo-plasmosis in immunosuppressed patients. Oxford University Press. 2015.
14. Robert-Gangneux F, Dardé ML. Epide-miology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012; 25:264-296.
15. Barratt J, Harkness J, Marriott D, et al. Importance of nonenteric protozoan in-fections in immunocompromised people. Clin Microbiol Rev. 2010;23;795-836.
16. Chehrazi-raffle A, Luu M, Yu Z, et al. Tox-oplasma gondii serology and outcomes after heart transplantation: contention in the lit-erature. Transplantation proceedings, 2015. Elsevier, 1949-1953.
17. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. BMJ. 2009, 339:b2535. 10.1136/bmj.b2535
18. Speich B, Croll D, Furst T, et al. Effect of sanitation and water treatment on intestinal protozoa infection: a systematic review and meta-analysis. Lancet Infect Dis. 2016;16:87–99.
19. Teimouri A, Keshavarz H, Mohtasebi S, et al. Intestinal parasites among food han-dlers in Iran: A systematic review and me-ta-analysis. Food Microbiol. 2020:103703.
20. Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of rec-ommendations. BMJ. 2004;328:1490.
21. Munn Z, Moola S, Lisy K, et al. Methodo-logical guidance for systematic reviews of observational epidemiological studies re-porting prevalence and cumulative inci-dence data. Int J Evid Base Healthc. 2015;13:147–153.
22. Hedges LV, Vevea JL. Fixed-and random-effects models in meta-analysis. Psychol Methods. 1998;3:486.
23. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002; 21:1539–1558.
24. Egger M, Smith GD, Schneider M, Mind-er C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.
25. Copas J, Shi JQ. Meta-analysis, funnel plots and sensitivity analysis. Biostatistics. 2000;1:247–262.
26. Abdollahi A, Shoar S, Sheikhbahaei S, Jafa-ri S. Sero-prevalence of cytomegalovirus and Toxoplasma infections among newly di-agnosed HIV patients in Iran, assessing the correlation with CD4+ cell counts. Iran J Pathol. 2013;8:81-88.
27. Alavi SM, Jamshidian R, Salmanzadeh S. Comparative study on Toxoplasma serology among HIV positive and HIV negative il-licit drug users in Ahvaz, Iran. Caspian J Intern Med. 2013;4(4):781
28. Izadi M, Jafari NJ, Poornaki AM, et al. De-tection of Toxoplasma gondii from clinical specimens of patients receiving renal transplant using ELISA and PCR. Nephro-Urology Monthly. 2013;5(5):983.
29. Soltani S, Khademvatan S, Saki J, Shahba-zian H. Detection of toxoplasmosis in re-nal transplant recipients by ELISA and PCR methods in Ahvaz, south-west of Iran. Jundishapur J Microbioly. 2013;6(9).
30. Fallahi S, Kazemi B, Bandehpour M, et al. Comparison of the RE and B1 gene for detection of Toxoplasma gondii infection in children with cancer. Parasitol Int. 2014;63(1):37-41.
31. Rostami A, Keshavarz H, Shojaee S, et al. Frequency of Toxoplasma gondii in HIV positive patients from West of Iran by ELISA and PCR. Iran J Parasitol. 2014;9(4):474.
32. Kalantari N, Ghaffari S, Bayani M, et al. Preliminary study on association between toxoplasmosis and breast cancer in Iran. Asian Pac J Trop Biomed. 2015;5(1):44-7.
33. Rahimi MT, Mahdavi SA, Javadian B, et al. High seroprevalence of Toxoplasma gondii antibody in HIV/AIDS individuals from North of Iran. Iran J Parasitol. 2015;10(4):584.
34. Barazesh A, Sarkari B, Sisakht FM, et al. Seroprevalence and molecular evaluation of toxoplasmosis in patients undergoing chemotherapy for malignancies in the Bu-shehr Province, Southwest Iran. Jundisha-pur J Microbiol. 2016;9(9).
35. Rasti S, Hassanzadeh M, Soliemani A, et al. Serological and molecular survey of toxo-plasmosis in renal transplant recipients and hemodialysis patients in Kashan and Qom regions, central Iran. Renal Failure. 2016;38(6):970-3.
36. Aghaee R, Saki SS, Didehdar M, et al. Epi-demiologic evaluation of toxoplasmosis and leading risk factors in HIV/AIDS pa-tients in Arak City, Iran. Australasian Med-ical Journal (Online). 2017;10(10):865-9.
37. Gharavi MJ, Roozbehani M, Mandeh Z. Detection of anti-Toxoplasma gondii antibod-ies in chronic myeloid leukemia and acute myeloid leukemia patients. Vet World. 2017;10(9):1063.
38. Hassanzadeh M, Rasti S, Hooshyar H, et al. Seroepidemiology of Toxoplasma gondii infection in immunodeficiency patients in Kashan and Qom during 2014-2015. KAUMS Journal (FEYZ). 2017;21(5):483-9.
39. Rezanezhad H, Sayadi F, Shadmand E, et al. Seroprevalence of Toxoplasma gondii among HIV patients in Jahrom, Southern Iran. Korean J Parasitol. 2017;55(1):99-103.
40. Saki J, Tavakoli S, Pedram M. Seropreva-lence and molecular evaluation of toxo-plasmosis in children with cancer in Khuzestan province, Southwest of Iran. J Parasit Dis. 2017;41(4):947-51.
41. Arefkhah N, Sarkari B, Afrashteh M, et al. Toxoplasma gondii: the prevalence and risk factors in HIV-infected patients in Fars province, southern Iran. Iran Red Crescent Med J. 2018;20(6):e66521.
42. Kalantari N, Rezanejad J, Tamadoni A, et al. Association between Toxoplasma gondii exposure and paediatrics haematological malignancies: a case–control study. Epi-demiol Infect. 2018;146(15):1896-902.
43. Nazari N, Bozorgomid A, Janbakhsh A, Bashiri F. Toxoplasma gondii and human immunodeficiency virus co-infection in western Iran: A cross sectional study. Asian Pac J Trop Med. 2018;11(1):58.
44. Ebrahim-Saraie HS, Heidari H, Mousavi S, et al. Toxoplasma gondii seroprevalence and related risk factors in patients with HIV in Iran. Archives of Hellenic Medi-cine/Arheia Ellenikes Iatrikes. 2018;35(3).
45. Shafieenia S, Saki J, Khademvatan S, et al. Molecular and Serological Evaluation of Toxoplasmosis in AIDS Cases in South-west Iran. Jundishapur J Microbiol. 2018;11(12).
46. Abdoli A, Barati M, Pirestani M, Dalimi A. Screening of toxoplasmosis in cancer pa-tients: a concern. Trop Doct. 2019;49(1):31-4.
47. Ahmadpour E, Pishkarie-Asl R, Spotin A, et al. Sero-molecular evaluation of Toxo-plasma gondii infection among HIV-positive patients. Trans R Soc Trop Med Hyg. 2019;113(12):771-5.
48. Arefkhah N, Hosseini SA, Karimzade R, et al. Seroprevalence and risk factors of Tox-oplasma gondii infection among cancer and hemodialysis patients in southwest Iran. Clin Epidemiology Glob Health. 2019;7(4):596-9.
49. Bavand A, Aghakhani A, Mohraz M, et al. Prevalence of Toxoplasma gondii antibodies and DNA in Iranian HIV Patients. Iran J Pathol. 2019;14(1):68.
50. Mousavi SA, Sajadi G, Ayatollahi J, et al. Evaluation of seroepidemiology of toxo-plasmosis in HIV+patients referring to the treatment centers of Yazd in 2014. Toloo-e-Behdasht. 2019;17(5):86-95.
51. Shokri F, Abbaszadeh R, Rrostamnezhad M, et al. Molecular and serological tech-niques to determine the acute and chronic phase of toxoplasmosis in HIV patients. J Babol Univ Medical Sci. 2019;21(1):140-6.
52. Bokharaei-Salim F, Esteghamati A, Khana-liha K, et al. Evaluation of a PCR assay for diagnosis of toxoplasmosis in serum and peripheral blood mononuclear cell among HIV/AIDS patients. J Parasit Dis. 2020;44(1):159-65.
53. Hosseini SA, Sharif M, Sarvi S, et al. Ge-netic characterization of Toxoplasma gondii in Iranian HIV positive patients using multi-locus nested-PCR-RFLP method. Parasit-ology. 2020;147(3):322-8.
54. Getso MI, Raissi V, Fasihi Karami M, et al. Toxoplasmosis among patients with can-cers and blood disorders in iran: Serologi-cal evaluation, risk factors and comparison with healthy individuals. J Chem Health Risks. 2021;11(3):271-82.
55. Hashemi SM, Mahmoodi S, Mehravaran A, et al. Serological and molecular evalua-tion of toxoplasmosis in patient undergo-ing chemotherapy for malignancies in southeast of Iran. Gene Reports. 2021;23:101163.
56. Hosseini SA, Sharif M, Sarvi S, et al. Tox-oplasmosis among cancer patients under-going chemotherapy: a population study based on the serological, molecular and epidemiological aspects. Trans R Soc Trop Med Hyg. 2021;115(6):677-86.
57. Rafati-Sajedi H, Majidi-Shad B, Jafari-Shakib R, et al. Serological Evaluation of Toxoplasmosis and Related Risk Factors Among HIV+/AIDS Patients in Northern Iran. Acta Parasitol. 2021;66(4):1417-23.
58. Nikbakht G, Behrouzi M, Mousavizadeh A, et al. Seroprevalence of Toxoplasma gondii infection among HIV-positive patients in Southwest Iran and associated risk factors: a case-control study. Trans R Soc Trop Med Hyg. 2022.
59. Ahmadpour E, Daryani A, Sharif M, et al. Toxoplasmosis in immunocompromised patients in Iran: a systematic review and meta-analysis. J Infect Dev Ctries. 2014;8(12):1503-10.
60. Wang ZD, Liu HH, Ma ZX, et al. Toxo-plasma gondii infection in immunocompro-mised patients: a systematic review and meta-analysis. Front Microbiol. 2017;8:389.
61. Wang ZD, Wang SC, Liu HH, et al. Preva-lence and burden of Toxoplasma gondii in-fection in HIV-infected people: a systemat-ic review and meta-analysis. The Lancet HIV. 2017;4(4):e177-e88.
62. Davarpanah M, Mehrbani D, NeyramI R, et al. Toxoplasmosis in HIV/AIDS pa-tients in Shiraz, southern Iran. Iran Red Crescent Med J. 9: 22-27.
63. Daryani A, Sharif M, Meigouni M. Sero-prevalence of IgG and IgM anti-Toxoplasma antibodies in HIV/AIDS pa-tients, northern Iran. Asian Pac J Trop Med. 2011;4(4):271-4.
64. Anvari D, Sharif M, Sarvi S, et al. Sero-prevalence of Toxoplasma gondii infection in cancer patients: a systematic review and meta-analysis. Microb Pathog. 2019;129:30-42.
65. Khurana S, Batra N. Toxoplasmosis in organ transplant recipients: Evaluation, implication, and prevention. Trop Parasi-tol. 2016;6(2):123.
66. Coster LOB. Parasitic infections in solid organ transplant recipients. Infect Dis Clin. 2013;27(2):395-427.
67. Stelzer S, Basso W, Silván JB, et al. Toxo-plasma gondii infection and toxoplasmosis in farm animals: Risk factors and economic impact. Food Waterborne Parasitol. 2019;15:e00037.
68. Liu Q, Wang ZD, Huang SY, Zhu XQ. Diagnosis of toxoplasmosis and typing of Toxoplasma gondii. Parasites Vectors. 2015; 8:292.
IssueVol 17 No 4 (2022) QRcode
SectionReview Article(s)
Toxoplasma gondii Immunocompromised patients HIV Aids Cancer patients Transplant recipients Iran

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
Teimouri A, Goudarzi F, Goudarzi K, Alimi R, Sahebi K, Forozand H, Keshavarz H. Toxoplasma gondii Infection in Immunocompromised Patients in Iran (2013-2022): A Systematic Review and Meta-Analysis. Iran J Parasitol. 2022;17(4):443-457.