Folia Parasitologica 72:024 (2025) | DOI: 10.14411/fp.2025.024

Special Issue: Association between type-2 diabetes and Toxoplasma gondii seropositivity: a systematic review and meta-analysis

Ashley Catchpole ORCID...1, Brinley N. Zabriskie ORCID...2, Bradley Embley1, Hannah Kharazi3, Rachelle Clarke3, Grace Templeton3, Christopher Hunt4, Shawn D. Gale ORCID...1, 3, Dawson W. Hedges1, 3
1 The Neuroscience Center, Brigham Young University, Provo, Utah;
2 The Department of Data Analytics and Information Systems, Utah State University, Logan, Utah;
3 The Department of Psychology, Brigham Young University, Provo, Utah;
4 The Department of Biophysics, Brigham Young University, Provo, Utah

A metabolic disease resulting in elevated blood glucose levels, type-2 diabetes affects approximately 462 million people globally. Although its prevalence appears to be increasing, type-2 diabetes has been associated with various potentially preventable risk factors, including infectious diseases. The protozoal infection with Toxoplasma gondii (Nicolle et Manceaux, 1908) has been associated with type-2 diabetes in two previous meta-analyses. Since the publication of the last meta-analysis supporting an association between type-2 diabetes and T. gondii, several new primary studies have investigated this association. In this meta-analysis, we sought to further characterise the association between type-2 diabetes and T. gondii. We identified primary studies using PubMed, Embase, Scopus and Web of Science. Twenty-five studies met our inclusion criteria for a total of 4,639 patients with type-2 diabetes and 3,492 controls. Eighteen primary studies found a positive association between type-2 diabetes and T. gondii, whereas seven did not. Using a frequentist random-effects meta-analysis model, we found an overall summary odds ratio of 2.77 (95-percent confidence interval: 2.03-3.76), suggesting that the odds people will have type-2 diabetes is 2.7 times higher for people seropositive for T. gondii. Future studies should investigate this association in additional geographical regions and explore whether this association is due to the immunosuppressive effects of type-2 diabetes or whether T. gondii directly or indirectly affects glucose metabolism, or both.

Keywords: diabetes mellitus, insulin-resistant diabetes, toxoplasmosis, protozoal infection, metabolic disorder

Received: July 15, 2024; Revised: May 31, 2025; Accepted: July 14, 2025; Published online: August 1, 2025  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Catchpole, A., Zabriskie, B.N., Embley, B., Kharazi, H., Clarke, R., Templeton, G., ... Hedges, D.W. (2025). Special Issue: Association between type-2 diabetes and Toxoplasma gondii seropositivity: a systematic review and meta-analysis. Folia Parasitologica72, Article 2025.024. https://doi.org/10.14411/fp.2025.024


This article is part of Special Issue,  Effects of Latent Toxoplasmosis: Three Decades of Studies.


Download citation

Attachments

Download fileFP_072_024_24_Suppl.pdf

File size: 263.92 kB

References

  1. Ahmed A.K., Kamal A.M., Abdel Fatah M.M., Abd Rabou R.A.M., Mahmoud H.A.H., Sanadeki M.M. 2023: Seroepidemiology of Toxoplasma gondii infection in diabetic patients and the impact of toxoplasmosis on diabetes associated complications in Minia City, Egypt. Infect. Dis. Trop. Med. 9: e1198.
  2. Ahuja S.K., Ahuja S.S., Thelmo W., Seymour A., Phelps K.R. 1993: Necrotizing pancreatitis and multisystem organ failure associated with toxoplasmosis in a patient with AIDS. Clin. Infect. Dis. 16: 432-434. Go to original source... Go to PubMed...
  3. Alvarado-Esquivel C., Loera-Moncivais N., Hernandez-Tinoco J., Sanchez-Anguiano L.F., Hernandez-Madrid G., Rabago-Sanchez E., Centeno-Tinoco M.M., Sandoval-Carrillo A.A., Salas-Pacheco J.M., Campos-Moreno O.V., Antuna-Salcido E.I. 2017: Lack of association between Toxoplasma gondii infection and diabetes mellitus: a matched case-control study in a Mexican population. J. Clin. Med. Res. 9: 508-511. Go to original source... Go to PubMed...
  4. Ashraf T., Sarker P.K., Hosen M.I., Rahman A., Hasan A., Rahman T. 2023: Association of chronic Toxoplasma gondii infection with pro-inflammatory cytokine interleukin (IL)-12 responses in type-2 diabetes mellitus patients of Bangladesh. J. Parasitol. Res. 2023: 3885160. Go to original source... Go to PubMed...
  5. Begg C.B., Mazumdar M. 1994: Operating characteristics of a rank correlation test for publication bias. Biometrics 50: 1088-1101. Go to original source...
  6. Berbudi A., Rahmadika N., Tjahjadi A.I., Ruslami R. 2020: Type 2 diabetes and its impact on the immune system. Curr. Diabetes Rev. 16: 442-449. Go to original source... Go to PubMed...
  7. Casqueiro J., Casqueiro J., Alves C. 2012: Infections in patients with diabetes mellitus: a review of pathogenesis. Ind. J. Endocrinol. Metab. 16 (Suppl 1): S27-36. Go to original source... Go to PubMed...
  8. Chávez-Reyes J., Escárcega-González C.E., Chavira-Suárez E., León-Buitimea A., Vázquez-León P., Morones-Ramírez J.R., Villalón C.M., Quintanar-Stephano A., Marichal-Cancino B.A. 2021: Susceptibility for some infectious diseases in patients with diabetes: the key role of glycemia. Front. Publ. Health 9: 559595. Go to original source... Go to PubMed...
  9. Chen L., Chen R., Wang H., Liang F. 2015: Mechanisms linking inflammation to insulin resistance. Int. J. Endocrinol. 2015: 508409. Go to original source... Go to PubMed...
  10. Dabirzadeh M., Sargazi M., Bagheri S. 2024: Seroepidemiology of Toxoplasma gondii in diabetic patients type 2 by enzyme-linked immunosorbent assay method in Zabol City, 2017-2018. J. Res. Med. Sci. 29: 19. Go to original source... Go to PubMed...
  11. Elkholy A.A., Omar R.E., Elbadawy A.M., Elawady M.A., Abou-Ouf E. 2022: Investigating the potential link between seroprevalence of Toxoplasma IgG and both types of diabetes mellitus in Benha City, Egypt. Parasitol. United J. 15: 195-201. Go to original source...
  12. Galaviz K.I., Narayan K.M.V., Lobelo F., Weber M.B. 2018: Lifestyle and the prevention of type 2 diabetes: a status report. Am. J. Lifestyle Med. 12: 4-20. Go to original source... Go to PubMed...
  13. Galicia-Garcia U., Benito-Vicente A., Jebari S., Larrea-Sebal A., Siddiqi H., Uribe K.B., Ostolaza H., Martín C. 2020: Pathophysiology of type 2 diabetes mellitus. Int. J. Mol. Sci. 21: 6275. Go to original source... Go to PubMed...
  14. Gokce C., Yazar S., Bayram F., Gundogan K., Yaman O., Sahin I. 2008: Anti-Toxoplasma gondii antibodies in type 2 diabetes. Natl. Med. J. India 21: 51.
  15. Hartung J., Knapp G. 2001a: On tests of the overall treatment effect in meta-analysis with normally distributed responses. Stat. Med. 20: 1771-1782. Go to original source... Go to PubMed...
  16. Hartung J., Knapp G. 2001b: A refined method for the meta-analysis of controlled clinical trials with binary outcome. Stat. Med. 20: 3875-3889. Go to original source... Go to PubMed...
  17. Hemida M.H., Shahat S.A.R., Bayoumy A.M.S., Mohammad K.A.H. 2017: Prevalence of toxoplasmosis among diabetic patients. Eur. J. Pharm. Med. Res. 4: 137-140.
  18. Inceboz M., Inceboz T. 2021: Toxoplasmosis and neuropsychological effects. Turkiye Parazitol. Derg. 45: 49-55. Go to original source... Go to PubMed...
  19. Ioannidis J.P., Trikalinos T.A. 2007: The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey. Can. Med. Assoc. J. 176: 1091-1096. Go to original source... Go to PubMed...
  20. Jalil M.B., Mohammed Ali M.N., Jihad I.A., Alabadi H.I. 2023: Seropositivity of anti-Toxoplasma gondii IgG among type 2 diabetes mellitus patients. Rom. J. Infect. Dis. 26: 111-115. Go to original source...
  21. Kalogeropoulos D., Sakkas H., Mohammed B., Vartholomatos G., Malamos K., Sreekantam S., Kanavaros P., Kalogeropoulos C. 2022: Ocular toxoplasmosis: a review of the current diagnostic and therapeutic approaches. Int. Ophthalmol. 42: 295-321. Go to original source... Go to PubMed...
  22. Khalili M., Mahami-Oskouei M., Shahbazi A., Safaiyan A., Mohammadzadeh-Gheshlaghi N., Mahami-Oskouei L. 2018: The correlation between serum levels of anti-Toxoplasma gondii antibodies and the risk of diabetes. Iran J. Parasitol. 13: 637-642.
  23. Khan M.A.B., Hashim M.J., King J.K., Govender R.D., Mustafa H., Al Kaabi J. 2020: Epidemiology of type 2 diabetes - global burden of disease and forecasted trends. J. Epidemiol. Glob. Health. 10: 107-111. Go to original source... Go to PubMed...
  24. Kiselar J.G., Wang X., Dubyak G.R., El Sanadi C., Ghosh S.K., Lundberg K., Williams W.M. 2015: Modification of beta-defensin-2 by dicarbonyls methylglyoxal and glyoxal inhibits antibacterial and chemotactic function in vitro. PLoS One 10: e0130533. Go to original source... Go to PubMed...
  25. Li Y.X., Xin H., Zhang X.Y., Wei C.Y., Duan Y.H., Wang H.F., Niu H.T. 2018: Toxoplasma gondii infection in diabetes mellitus patients in China: seroprevalence, risk factors, and case-control studies. Biomed. Res. Int. 2018: 4723739. Go to original source... Go to PubMed...
  26. Majidiani H., Dalvand S., Daryani A., Galvan-Ramirez M.L., Foroutan-Rad M. 2016: Is chronic toxoplasmosis a risk factor for diabetes mellitus? A systematic review and meta-analysis of case-control studies. Braz. J. Infect. Dis. 20: 605-609. Go to original source... Go to PubMed...
  27. Mariuz P., Bosler E.M., Luft B.J. 1997: Toxoplasma pneumonia. Semin. Respir. Infect. 12: 40-43.
  28. Mohamed G.A., Ez Eldeen M.E., Elossily N.A., Gaber M., Hassan T.M., Mahran Z.G., Hetta H.F., Abdel Aziz E.M. 2020: Anti-Toxoplasma IgG level in type 2 diabetic patients: does it affect glycemic control? Egypt. J. Immunol. 27: 119-127.
  29. Mohammed K. 2025: The possible association between chronic toxoplasmosis and type-2 diabetes mellitus in women: a case-control study. Cureus 17: e79120. Go to original source... Go to PubMed...
  30. Mohammed T., Yaseen A.N., Aldabagh A.H. 2020: Evaluation of soluble PD-1 and PD-L1 Iraqi type 2 diabetes mellitus (T2DM) patients with chronic toxoplasmosis. Medico-Legal Update 20: 477-481.
  31. Molan A.L., Ismail M.H. 2021: Is there a positive association between Toxoplasma gondii seropositivity and obesity in diabetic patients? Ann. Parasitol. 67: 537-542.
  32. Molan A., Nosaka K., Hunter M., Wang W. 2020: The association between Toxoplasma gondii and type 2 diabetes mellitus: a systematic review and meta-analysis of human case-control studies. Bull. Natl. Res. Centre 44: 1-8. Go to original source...
  33. Montoya J.G., Liesenfeld O. 2004: Toxoplasmosis. Lancet 363: 1965-1976. Go to original source... Go to PubMed...
  34. Nassief Beshay E.V., El-Refai S.A., Helwa M.A., Atia A.F., Dawous M.M. 2018: Toxoplasma gondii as a possible causative pathogen of type-1 diabetes mellitus: evidence from case-control and experimental studies. Exp. Parasitol. 188: 93-101. Go to original source... Go to PubMed...
  35. Oz H.S. 2014: Toxoplasmosis, pancreatitis, obesity and drug discovery. Pancreat. Disord. Ther. 4: 138.
  36. Özçelik S., Alim M., Ozpinar N. 2020: Detection of Toxoplasma gondii infection among diabetic patients in Turkey. Clin. Epidemiol. Glob. Health 8: 899-902. Go to original source...
  37. Page M.J., McKenzie J.E., Bossuyt P.M., Boutron I., Hoffmann T.C., Mulrow C.D., Shamseer L., Tetzlaff J.M., Akl E.A., Brennan S.E., Chou R., Glanville J., Grimshaw J.M., Hrobjartsson A., Lalu M.M., Li T., Loder E.W., Mayo-Wilson E., McDonald S., McGuinness L.A., Stewart L.A., Thomas J., Tricco A.C., Welch V.A., Whiting P., Moher D. 2021: The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. J. Clin. Epidemiol. 134: 178-189. Go to original source... Go to PubMed...
  38. Park E.A., Han I.H., Kim J.H., Park S.J., Ryu J.S., Ahn M.H. 2019: Production of inflammatory cytokines and nitric oxide by human mast cells incubated with Toxoplasma gondii lysate. Kor. J. Parasitol. 57: 201-206. Go to original source... Go to PubMed...
  39. Peters J.L., Sutton A.J., Jones D.R., Abrams K.R., Rushton L. 2006: Comparison of two methods to detect publication bias in meta-analysis. JAMA 295: 676-680. Go to original source... Go to PubMed...
  40. Peters J.L., Sutton A.J., Jones D.R., Abrams K.R., Rushton L. 2008: Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J. Clin. Epidemiol. 61: 991-996. Go to original source... Go to PubMed...
  41. Pradeepa R., Mohan V. 2017: Prevalence of type 2 diabetes and its complications in India and economic costs to the nation. Eur. J. Clin. Nutr. 71: 816-824. Go to original source... Go to PubMed...
  42. Prandota J. 2013: T gondii infection acquired during pregnancy and/or after birth may be responsible for the development of both type 1 and 2 diabetes mellitus. J. Diabetes Metabol. 4: 1000241. Go to original source...
  43. Qudus J., Haider K. 2019: The relation of Toxoplasma gondii with tumor-necrotizing factor-α in type II diabetic patients. Res. J. Pharm. Technol. 12: 4817-4821. Go to original source...
  44. R Core Team (Ed.) 2024: A Language and Environment for Statistical Computing. https://www.r-project.org/ 2025.
  45. Saeed S.A., Al-Aubaidi I.K. 2024: Prevalence of toxoplasmosis in Iraqi patients with diabetic type 2. Roman. J. Infect. Dis. 27: 144-150. Go to original source...
  46. Saheb E. 2017: Detection of toxoplasmosis infection in diabetic patients. Diyala J. Med. 12: 70-74.
  47. Saki J., Khodkar I., Shandnoosh F., Safi M., Ghadiri A., Shaefieenia S. 2022: Study of toxoplasmosis in type 2 diabetic patients using ELISA and B1 nested-PCR methods. Ann. Parasitol. 68: 367-373.
  48. Salem D.A., Salem N.A., Hendawy S.R. 2021: Association between Toxoplasma gondii infection and metabolic syndrome in obese adolescents: a possible immune-metabolic link. Parasitol. Int. 83: 102343. Go to original source... Go to PubMed...
  49. Salman O.D., Merdaw M.A.Z., Almaliky A.A. 2023: The probable association between Type 2 diabetes mellitus and Toxoplasma gondii infection. Int. J. Drug Del. Tech. 13: 131-135. Go to original source...
  50. Shamsinia S., Dalimi A., Pirestani M. 2019: Is toxoplasmosis a risk factor in diabetic patients in Tehran? Infect. Epidemiol. Microbiol. 5: 49-59.
  51. Sidik K., Jonkman J.N. 2002: A simple confidence interval for meta-analysis. Stat. Med. 21: 3153-3159. Go to original source... Go to PubMed...
  52. Smith N.C., Goulart C., Hayward J.A., Kupz A., Miller C.M., van Dooren G.G. 2021: Control of human toxoplasmosis. Int. J. Parasitol. 51: 95-121. Go to original source... Go to PubMed...
  53. Soltani S., Tavakoli S., Sabaghan M., Kahvaz M.S., Pashmforosh M., Foroutan M. 2021: The probable association between chronic Toxoplasma gondii infection and type 1 and type 2 diabetes mellitus: a case-control study. Interdiscipl. Perspect. Infect. Dis. 2021: 2508780. Go to original source... Go to PubMed...
  54. Viechtbauer W. 2010: Conducting meta-analyses in R with the metafor package. J. Statist. Software 36: 1-48. Go to original source...
  55. Wells G. 2001: The Newcastle-Ottawa Scale (NOS) for assessing the quality of non randomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
  56. Xiao J., Savonenko A., Yolken R.H. 2022: Strain-specific pre-existing immunity: a key to understanding the role of chronic Toxoplasma infection in cognition and Alzheimer's diseases? Neurosci. Biobehav. Rev. 137: 104660. Go to original source... Go to PubMed...
  57. Younis E.Z., Elamami A.H. 2018: Anti-Toxoplasma gondii IgG, IgM, and IgA among type-2 diabetic patients in Benghazi Libya: a comparison study. J. Immunol. Microbiol. 2: 2.