{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,25]],"date-time":"2026-01-25T12:14:43Z","timestamp":1769343283394,"version":"3.49.0"},"reference-count":36,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,3,2]],"date-time":"2023-03-02T00:00:00Z","timestamp":1677715200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Type-1 diabetes, an autoimmune disease characterized by damage to pancreatic insulin-producing beta cells, is associated with adverse renal, retinal, cardiovascular, and cognitive outcomes, possibly including dementia. Moreover, the protozoal parasite Toxoplasma gondii has been associated with type-1 diabetes. To better characterize the association between type-1 diabetes and Toxoplasma gondii infection, we conducted a systematic review and meta-analysis of published studies that evaluated the relationship between type-1 diabetes and Toxoplasma gondii infection. A random-effects model based on nine primary studies (total number of participants = 2655) that met our inclusion criteria demonstrated a pooled odds ratio of 2.45 (95% confidence interval, 0.91\u20136.61). Removing one outlying study increased the pooled odds ratio to 3.38 (95% confidence interval, 2.09\u20135.48). These findings suggest that Toxoplasma gondii infection might be positively associated with type-1 diabetes, although more research is needed to better characterize this association. Additional research is required to determine whether changes in immune function due to type-1 diabetes increase the risk of infection with Toxoplasma gondii, infection with Toxoplasma gondii increases the risk of type-1 diabetes, or both processes occur.<\/jats:p>","DOI":"10.3390\/ijerph20054436","type":"journal-article","created":{"date-parts":[[2023,3,2]],"date-time":"2023-03-02T03:29:00Z","timestamp":1677727740000},"page":"4436","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Association between Toxoplasma gondii Infection and Type-1 Diabetes Mellitus: A Systematic Review and Meta-Analysis"],"prefix":"10.3390","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6438-083X","authenticated-orcid":false,"given":"Ashley","family":"Catchpole","sequence":"first","affiliation":[{"name":"The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2621-7000","authenticated-orcid":false,"given":"Brinley N.","family":"Zabriskie","sequence":"additional","affiliation":[{"name":"The Department of Statistics, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pierce","family":"Bassett","sequence":"additional","affiliation":[{"name":"The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bradley","family":"Embley","sequence":"additional","affiliation":[{"name":"The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David","family":"White","sequence":"additional","affiliation":[{"name":"The Department of Micro and Molecular Biology, Brigham Young University, Provo, UT 84602, USA"},{"name":"The Department of Psychology, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8989-0964","authenticated-orcid":false,"given":"Shawn D.","family":"Gale","sequence":"additional","affiliation":[{"name":"The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA"},{"name":"The Department of Psychology, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dawson","family":"Hedges","sequence":"additional","affiliation":[{"name":"The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA"},{"name":"The Department of Psychology, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1503\/cmaj.060244","article-title":"Type 1 diabetes: Pathogenesis and prevention","volume":"175","author":"Gillespie","year":"2006","journal-title":"Can. Med. Assoc. J."},{"key":"ref_2","unstructured":"(2022, December 01). World Health Organization. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/diabetes."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.ecl.2010.05.011","article-title":"Epidemiology of type 1 diabetes","volume":"39","author":"Maahs","year":"2010","journal-title":"Endocrinol. Metab. Clin. N. Am."},{"key":"ref_4","first-page":"504","article-title":"Long-term complications of type 1 diabetes: What do we know and what do we need to understand?","volume":"73","author":"Piona","year":"2021","journal-title":"Minerva Pediatr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"29","DOI":"10.3233\/JAD-161250","article-title":"Type 1 diabetes mellitus and cognitive impairments: A systematic review","volume":"57","author":"Li","year":"2017","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.jcv.2017.09.003","article-title":"Type 1 diabetes and viral infections: What is the relationship?","volume":"96","author":"Principi","year":"2017","journal-title":"J. Clin. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1023\/A:1024256305963","article-title":"Infections and risk of type 1 diabetes in childhood: A population-based case-control study","volume":"18","author":"Altobelli","year":"2003","journal-title":"Eur. J. Epidemiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"8881908","DOI":"10.1155\/2021\/8881908","article-title":"High prevalence of Toxoplasma gondii infection in type I diabetic patients","volume":"2021","author":"Asgari","year":"2021","journal-title":"J. Parasitol. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2508780","DOI":"10.1155\/2021\/2508780","article-title":"The probable association between chronic Toxoplasma gondii infection and type 1 and type 2 diabetes mellitus: A case-control study","volume":"2021","author":"Soltani","year":"2021","journal-title":"Interdiscip. Perspect. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1016\/S0140-6736(04)16412-X","article-title":"Toxoplasmosis","volume":"363","author":"Montoya","year":"2004","journal-title":"Lancet"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3095","DOI":"10.1080\/21505594.2021.2012346","article-title":"The pathogenicity and virulence of Toxoplasma gondii","volume":"12","author":"Sanchez","year":"2021","journal-title":"Virulence"},{"key":"ref_12","first-page":"305","article-title":"Seroprevalence of Toxoplasma gondii infections among patients with autoimmune diseases","volume":"33","author":"Cao","year":"2020","journal-title":"Zhongguo Xuexichongbing Fangzhi Zazhi"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.bjid.2016.09.002","article-title":"Is chronic toxoplasmosis a risk factor for diabetes mellitus? A systematic review and meta-analysis of case-control studies","volume":"20","author":"Majidiani","year":"2016","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.exppara.2018.04.007","article-title":"Toxoplasma gondii as a possible causative pathogen of type-1 diabetes mellitus: Evidence from case-control and experimental studies","volume":"188","author":"Helwa","year":"2018","journal-title":"Exp. Parasitol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.metabol.2021.154795","article-title":"Understanding the increased risk of infections in diabetes: Innate and adaptive immune responses in type 1 diabetes","volume":"121","author":"Janssen","year":"2021","journal-title":"Metab. Clin. Exp."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/IAI.00398-18","article-title":"Chronic Toxoplasma gondii infection induces anti-N-methyl-d-aspartate receptor autoantibodies and associated behavioral changes and neuropathology","volume":"86","author":"Li","year":"2018","journal-title":"Infect. Immun."},{"key":"ref_17","unstructured":"Higgins, J.P.T., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M.J., and Welch, V.A. (2022). Cochrane Handbook for Systematic Reviews of Interventions, Cochrane. Available online: www.training.cochrane.org\/handbook."},{"key":"ref_18","unstructured":"(2022, November 12). R: A Language and Environment for Statistical Computing. Available online: https:\/\/www.R-project.org\/."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1136\/ebmental-2019-300117","article-title":"How to perform a meta-analysis with R: A practical tutorial","volume":"22","author":"Balduzzi","year":"2019","journal-title":"Evid. Based Ment. Health"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3875","DOI":"10.1002\/sim.1009","article-title":"A refined method for the meta-analysis of controlled clinical trials with binary outcome","volume":"20","author":"Hartung","year":"2001","journal-title":"Stat. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3153","DOI":"10.1002\/sim.1262","article-title":"A simple confidence interval for meta-analysis","volume":"21","author":"Sidik","year":"2002","journal-title":"Stat. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1111\/j.1749-6632.2009.04619.x","article-title":"Anti-infectious antibodies and autoimmune-associated autoantibodies in patients with type I diabetes mellitus and their close family members","volume":"1173","author":"Krause","year":"2009","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_23","first-page":"414","article-title":"Seroepidemiological survey of Toxoplasma gondii infections in patients with diabetes mellitus in Hangzhou City","volume":"33","author":"Xia","year":"2021","journal-title":"Zhongguo Xuexichongbing Fangzhi Zazhi"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4723739","DOI":"10.1155\/2018\/4723739","article-title":"Toxoplasma gondii infection in diabetes mellitus patients in China: Seroprevalence, risk factors, and case-control studies","volume":"2018","author":"Li","year":"2018","journal-title":"BioMed Res. Int."},{"key":"ref_25","first-page":"637","article-title":"The correlation between serum levels of anti-Toxoplasma gondii antibodies and the risk of diabetes","volume":"13","author":"Khalili","year":"2018","journal-title":"Iran. J. Parasitol."},{"key":"ref_26","first-page":"51","article-title":"Anti-Toxoplasma gondii antibodies in type 2 diabetes","volume":"21","author":"Gokce","year":"2008","journal-title":"Natl. Med. J."},{"key":"ref_27","first-page":"537","article-title":"Is there a positive association between Toxoplasma gondii seropositivity and obesity in diabetic patients?","volume":"67","author":"Molan","year":"2021","journal-title":"Ann. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1771","DOI":"10.1002\/sim.791","article-title":"On tests of overall treatment effect in meta-analysis with normally distributed responses","volume":"20","author":"Hartung","year":"2001","journal-title":"Stat. Med."},{"key":"ref_29","unstructured":"Deeks, J.J., Higgins, J.P.T., and Altman, D.G. (2021). Cochrane Handbook for Systematic Review of Interventions, Cochrane. version 6.2."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"113089","DOI":"10.1016\/j.biopha.2022.113089","article-title":"COVID-19 and diabetes: Association intensify risk factors for morbidity and mortality","volume":"151","author":"Sharma","year":"2022","journal-title":"Biomed. Pharmacother."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/S0891-5520(05)70153-7","article-title":"Infections in diabetes","volume":"15","author":"Calvet","year":"2001","journal-title":"Infect. Dis. Clin. N. Am."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1002\/(SICI)1096-9136(199701)14:1<29::AID-DIA300>3.0.CO;2-V","article-title":"Impaired leucocyte functions in diabetic patients","volume":"14","author":"Delamaire","year":"1997","journal-title":"Diabetic Med."},{"key":"ref_33","first-page":"187","article-title":"Impaired immune responses in diabetes mellitus: Analysis of the factors and mechanisms involved. Relevance to the increased susceptibility of diabetic patients to specific infections","volume":"18","author":"Moutschen","year":"1992","journal-title":"Diabete Metab."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4172\/2155-6156.1000241","article-title":"Gondii infection acquired during pregnancy and\/or after birth may be responsible for development of both type 1 and 2 diabetes mellitus","volume":"4","author":"Prandota","year":"2013","journal-title":"J. Diabetes. Metab."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1080\/08820130802205886","article-title":"Autoimmune disease during pregnancy and the microchimerism legacy of pregnancy","volume":"37","author":"Nelson","year":"2008","journal-title":"Immunol. Invest."},{"key":"ref_36","first-page":"138","article-title":"Toxoplasmosis, pancreatitis, obesity and drug discovery","volume":"4","author":"Oz","year":"2014","journal-title":"Pancreat. Disord. Ther."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/20\/5\/4436\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:45:52Z","timestamp":1760121952000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/20\/5\/4436"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,2]]},"references-count":36,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["ijerph20054436"],"URL":"https:\/\/doi.org\/10.3390\/ijerph20054436","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,2]]}}}