{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T14:10:48Z","timestamp":1790518248496,"version":"4.1.0"},"reference-count":48,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T00:00:00Z","timestamp":1666224000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:p>Livestock animals, such as swine, are an important source of <jats:italic>Toxoplasma gondii<\/jats:italic> in the human population. Currently, there is limited knowledge regarding the potential influence that the <jats:italic>T. gondii<\/jats:italic> genotype might exert on establishing infection in swine. Herein, we investigated the role of 2 <jats:italic>T. gondii<\/jats:italic> isolates, type II and III, representative of the genotypes circulating in Europe, in the immune responses and infection dynamics in piglets. Recently obtained oocysts (10<jats:sup>3<\/jats:sup>) from the <jats:italic>T. gondii<\/jats:italic> field isolates TgShSp1 (type II, ToxoDB genotype #3) and TgShSp24 (type III, #2) were used for oral infection. Thirteen 50-day-old female piglets of the Landrace-Large White crossbreed were randomly allocated into three different groups: Group 1 (G1, n=5), inoculated with TgShSp1; Group 2 (G2, n=5), inoculated with TgShSp24; and Group 3 (G3, n=3), a non-infected control group. Clinical signs were monitored daily until 42 days post-infection (dpi) when piglets were euthanized. Blood samples were collected weekly to test the cellular immune response in parasite-stimulated peripheral blood and specific IgG, IgG1 and IgG2, responses in sera. Parasite distribution and burden were evaluated in target tissues using a mouse bioassay and quantitative RT\u2212PCR (qPCR). Apathy and a moderate decrease in feed consumption were observed in G1 and G2 piglets between 5 and 8 dpi, coinciding with fever (&amp;gt;40\u00b0C). G2 piglets had higher temperatures for a longer duration. Using mouse bioassay and qPCR, the detection frequency was higher in G2 <jats:italic>vs.<\/jats:italic> G1, and the highest parasite burdens in target tissues were also found in G2. Seroconversion was detected at 14 dpi in both infected groups, but higher antibody levels were observed in G2 piglets. Cytokine analyses revealed the production of IL-8, IL-1\u03b2 and IFN-\u0264 from 7 dpi in both infected groups. Moreover, IL-12 was produced from 7 dpi in G1 and from 14 dpi in G2. Levels of IL-8 were higher in G2, but IL-1\u03b2, IL-12 and IFN-\u0264 were higher in G1 at 14 dpi. This cytokine profile reveals a predominant proinflammatory response that could be involved in limiting <jats:italic>T. gondii<\/jats:italic> infection in piglets, although it is more efficient against TgShSp1 type II-driven infection.<\/jats:p>","DOI":"10.3389\/fimmu.2022.1021556","type":"journal-article","created":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T08:55:56Z","timestamp":1666256156000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["Archetypal type II and III Toxoplasma gondii oocysts induce different immune responses and clinical outcomes in experimentally infected piglets"],"prefix":"10.3389","volume":"13","author":[{"given":"Andrea","family":"Largo-de la Torre","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlos","family":"Diezma-D\u00edaz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rafael","family":"Calero-Bernal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriela","family":"Atencia-Cibreiro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto","family":"S\u00e1nchez-S\u00e1nchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ignacio","family":"Ferre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Javier","family":"Regidor-Cerrillo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luis Miguel","family":"Ortega-Mora","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,10,20]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1016\/s0020-7519(00)00124-7","article-title":"Toxoplasma gondii: From animals to humans","volume":"30","author":"Tenter","year":"2000","journal-title":"Int J Parasitol"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.4315\/0362-028x.jfp-14-328","article-title":"Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption","volume":"78","author":"Guo","year":"2015","journal-title":"J Food Prot"},{"key":"B3","first-page":"1","volume-title":"Toxoplasmosis of animals and humans, 3rd ed","author":"Dubey","year":"2022"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2020.109185","article-title":"All about Toxoplasma gondii infections in pigs: 2009\u20132020","volume":"288","author":"Dubey","year":"2020","journal-title":"Vet Parasitol"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.2903\/j.efsa.2011.2351","article-title":"Scientific opinion on the public health hazards to be covered by inspection of meat (swine)","volume":"9","author":"Andreoletti","year":"2011","journal-title":"EFSA J"},{"key":"B6","volume-title":"Toxoplasmosis of animals and humans (2nd ed.)","author":"Dubey","year":"2010"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1016\/j.fm.2013.08.011","article-title":"Brain is the predilection site of Toxoplasma gondii in experimentally inoculated pigs as revealed by magnetic capture and real-time PCR","volume":"38","author":"Jur\u00e1nkov\u00e1","year":"2014","journal-title":"Food Microbiol"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijpara.2017.12.009","article-title":"Pork as a source of transmission of Toxoplasma gondii to humans: A parasite burden study in pig tissues after infection with different strains of Toxoplasma gondii as a function of time and different parasite stages","volume":"48","author":"Gisbert Algaba","year":"2018","journal-title":"Int J Parasitol"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms8040518","article-title":"Q. iTRAQ-based quantitative proteomics analysis identifies host pathways modulated during Toxoplasma gondii infection in swine","volume":"8","author":"He","year":"2020","journal-title":"Microorganisms"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1177\/104063871002200318","article-title":"An outbreak of lethal toxoplasmosis in pigs in the gansu province of China","volume":"22","author":"Li","year":"2010","journal-title":"J Vet Diagn Invest"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1007\/s00436-016-4999-0","article-title":"Acute toxoplasmosis in pigs in Brazil caused by Toxoplasma gondii genotype Chinese 1","volume":"115","author":"Olinda","year":"2016","journal-title":"Parasitol Res"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1177\/030098589902700605","article-title":"Lesions in fetal pigs with transplacentally-induced toxoplasmosis","volume":"27","author":"Dubey","year":"1990","journal-title":"Vet Pathol"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1016\/j.parint.2014.11.017","article-title":"Involvement of Toxoplasma gondii in reproductive disorders in Swiss pig farms","volume":"64","author":"Basso","year":"2015","journal-title":"Parasitol Int"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2022.842595","article-title":"Toxoplasma gondii genotyping: A closer look into Europe","volume":"12","author":"Fern\u00e1ndez-Escobar","year":"2022","journal-title":"Front Cell Infect Microbiol"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/172.6.1561","article-title":"Toxoplasma gondii comprises three clonal lineages: Correlation of parasite genotype with human disease","volume":"172","author":"Howe","year":"1995","journal-title":"J Infect Dis"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1128\/jcm.35.6.1411-1414.1997","article-title":"Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis","volume":"35","author":"Howe","year":"1997","journal-title":"J Clin Microbiol"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2010.11.046","article-title":"Prevalence and genotypes of Toxoplasma gondii in feline faeces (oocysts) and meat from sheep, cattle and pigs in Switzerland","volume":"177","author":"Berger-Schoch","year":"2011","journal-title":"Vet Parasitol"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.3389\/fvets.2020.604782","article-title":"Isolation, genotyping, and mouse virulence characterization of Toxoplasma gondii from free ranging Iberian pigs","volume":"7","author":"Fern\u00e1ndez-Escobar","year":"2020","journal-title":"Front Vet Sci"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1186\/s13567-021-00953-7","article-title":"In vivo and in vitro models show unexpected degrees of virulence among Toxoplasma gondii type II and III isolates from sheep","volume":"52","author":"Fern\u00e1ndez-Escobar","year":"2021","journal-title":"Vet Res"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2018.00436","article-title":"Virulence in mice of a Toxoplasma gondii type II isolate does not correlate with the outcome of experimental infection in pregnant sheep","volume":"8","author":"S\u00e1nchez-S\u00e1nchez","year":"2019","journal-title":"Front Cell Infect Microbiol"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00232","article-title":"Strain- and dose-dependent reduction of toxoplasma gondii burden in pigs is associated with interferon-gamma production by CD8+ lymphocytes in a heterologous challenge model","volume":"7","author":"Jennes","year":"2017","journal-title":"Front Cell Infect Microbiol"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1186\/s13071-020-04275-z","article-title":"Isolation and genetic characterization of Toxoplasma gondii in Spanish sheep flocks","volume":"13","author":"Fern\u00e1ndez-Escobar","year":"2020","journal-title":"Parasites Vectors"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2017.07.029","article-title":"A new lyophilized tachyzoite based ELISA to diagnose Besnoitia spp. infection in bovids and wild ruminants improves specificity","volume":"244","author":"Garc\u00eda-Lunar","year":"2017","journal-title":"Vet Parasitol"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1017\/s003118200800509x","article-title":"M. isolation and genetic characterization of Neospora caninum from asymptomatic calves in Spain","volume":"135","author":"Regidor-Cerrillo","year":"2008","journal-title":"Parasitology"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1177\/1040638712452730","article-title":"Application of quantitative real-time polymerase chain reaction for the diagnosis of toxoplasmosis and enzootic abortion of ewes","volume":"24","author":"Gutierrez","year":"2012","journal-title":"J Vet Diagn Invest"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1016\/j.parint.2019.101935","article-title":"A Toxoplasma gondii strain isolated in Okinawa, Japan shows high virulence in microminipigs","volume":"72","author":"Taniguchi","year":"2019","journal-title":"Parasitol Int"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2022.868727","article-title":"Unifying virulence evaluation in Toxoplasma gondii: A timely task","volume":"28","author":"Calero-Bernal","year":"2022","journal-title":"Front Cell Infect Microbiol"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2011.11.002","article-title":"The pig: A model for human infectious diseases","volume":"20","author":"Meurens","year":"2012","journal-title":"Trends Microbiol"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2020.580425","article-title":"Influence of the host and parasite strain on the immune response during Toxoplasma infection","volume":"10","author":"Mukhopadhyay","year":"2020","journal-title":"Front Cell Infect Microbiol"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1038\/359082a0","article-title":"Virulent strains of Toxoplasma gondii comprise a single clonal lineage","volume":"359","author":"Sibley","year":"1992","journal-title":"Nature"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1128\/msystems.01196-21","article-title":"The extracellular milieu of Toxoplasma \u2018s lytic cycle drives Lab adaptation, primarily by transcriptional reprogramming","volume":"6","author":"Primo","year":"2021","journal-title":"mSystems"},{"key":"B32","doi-asserted-by":"publisher","first-page":"438","DOI":"10.2307\/3284082","article-title":"Infectivity of low numbers of Toxoplasma gondii oocysts to pigs","volume":"82","author":"Dubey","year":"1996","journal-title":"J Parasitol"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1016\/j.exppara.2006.02.001","article-title":"Toxoplasma gondii: Detection by mouse bioassay, histopathology, and polymerase chain reaction in tissues from experimentally infected pigs","volume":"113","author":"Garcia","year":"2006","journal-title":"Exp Parasitol"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1016\/j.rvsc.2017.07.02220","article-title":"The use of ELISA, nPCR and qPCR for diagnosis of ocular toxoplasmosis in experimentally infected pigs","volume":"115","author":"Garcia","year":"2017","journal-title":"Res Vet Sci"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1186\/s13567-015-0177-0","article-title":"Vaccination of pigs with the S48 strain of Toxoplasma gondii \u2013 safer meat for human consumption","volume":"46","author":"Burrells","year":"2015","journal-title":"Vet Res"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1016\/j.fm.2017.04.007","article-title":"Lack of viable parasites in cured \u2018Parma ham\u2019 (PDO), following experimental Toxoplasma gondii infection of pigs","volume":"66","author":"Genchi","year":"2017","journal-title":"Food Microbiol"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms8040518","article-title":"iTRAQ-based quantitative proteomics analysis identifies host pathways modulated during Toxoplasma gondii infection in swine","volume":"8","author":"He","year":"2020","journal-title":"Microorganisms"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetpar.2019.108963","article-title":"Cell mediated and innate immune responses in pigs following vaccination and challenge with Toxoplasma parasites","volume":"275","author":"Bartley","year":"2019","journal-title":"Vet Parasitol"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-019-5458-y","article-title":"Comparison of splenocyte microRNA expression profiles of pigs during acute and chronic toxoplasmosis","volume":"20","author":"Hou","year":"2019","journal-title":"BMC Genomics"},{"key":"B40","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.ijfoodmicro.2010.02.027","article-title":"Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR","volume":"139","author":"Opsteegh","year":"2010","journal-title":"Int J Food Microbiol"},{"key":"B41","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.vetpar.2011.02.015","article-title":"IFN-\u03b3 expression and infectivity of toxoplasma infected tissues are associated with an antibody response against GRA7 in experimentally infected pigs","volume":"179","author":"Verhelst","year":"2011","journal-title":"Vet Parasitol"},{"key":"B42","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.vetpar.2014.11.014","article-title":"Interferon-gamma expression and infectivity of Toxoplasma infected tissues in experimentally infected sheep in comparison with pigs","volume":"207","author":"Verhelst","year":"2015","journal-title":"Vet Parasitol"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2020.00161","article-title":"Early kinetics of intestinal infection and immune responses to two Toxoplasma gondii strains in pigs","volume":"10","author":"Rahman","year":"2020","journal-title":"Front Cell Infect Microbiol"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1007\/s00436-021-07204-w","article-title":"The role of IL-12 in stimulating NK cells against Toxoplasma gondii infection: A mini-review","volume":"120","author":"Mahmoudzadeh","year":"2021","journal-title":"Parasitol Res"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1186\/1756-3305-6-273","article-title":"Toxoplasma gondii prevalence in food animals and rodents in different regions of China: Isolation, genotyping and mouse pathogenicity","volume":"6","author":"Wang","year":"2013","journal-title":"Parasites Vectors"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1128\/iai.01615-14","article-title":"Toxoplasma gondii induction of CD40 on infected macrophages enhances interleukin-12 responses","volume":"82","author":"Morgado","year":"2014","journal-title":"Infect Immun"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.0900640","article-title":"Early response of mucosal epithelial cells during Toxoplasma gondii infection","volume":"183","author":"Ju","year":"2009","journal-title":"J Immunol"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1008586","article-title":"Toxoplasma GRA15 and GRA24 are important activators of the host innate immune response in the absence of TLR11","volume":"16","author":"Mukhopadhyay","year":"2020","journal-title":"PloS Pathog"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2022.1021556\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,20]],"date-time":"2022-10-20T08:56:00Z","timestamp":1666256160000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2022.1021556\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,20]]},"references-count":48,"alternative-id":["10.3389\/fimmu.2022.1021556"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2022.1021556","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,20]]},"article-number":"1021556"}}