Abstract
This study aimed to determine the nPCR-RFLP genotypes of newly obtained T. gondii isolates from human congenital toxoplasmosis cases in Argentina and to determine their allelic profiles for virulence genes ROP18/ROP5. In addition, the ROP18/ROP5 profiles were also determined for previously characterized T. gondii samples. Isolation from congenital toxoplasmosis cases was carried out in mouse bioassay from two placentas (P1 and P2). Genotyping for the new human isolates was performed by nPCR-RFLP using 10 markers. The samples analyzed for ROP18/ROP5 included the two newly obtained isolates (from the congenital toxoplasmosis cases) and nine previously genotyped T. gondii DNA samples from humans and chickens. The results for P1 and P2 named as TgHm18-02Arg and TgHm19-01Arg showed ToxoDB genotypes #14 (non-archetypal) and #2 (clonal type III), respectively. Non-archetypal #14 has been isolated from human cases before in Argentina. However, this is the first report of T. gondii clonal type III in a human case in the country. The ROP18/ROP5 combination was detected in nine samples: 3/3 (n = 1), 4/3 (n = 4), 4/4 (n = 3), and 3–4/4 (n = 1). Notably, the 4/4 profile was identified for the first time and exclusively in T. gondii samples from Misiones province (which borders southern Brazil). Further studies are required to corroborate the regionalization of the ROP18/ROP5 profiles in Argentina.
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References
Ajzenberg D, Cogné N, Paris L, Bessières MH, Thulliez P, Filisetti D, Pelloux H, Marty P, Dardé ML (2002) Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings. J Infect Dis 186(5):684–689. https://doi.org/10.1086/342663
Behnke MS, Khan A, Lauron EJ, Jimah JR, Wang Q, Tolia NH (2015) Rhoptry proteins ROP5 and ROP18 are major murine virulence factors in genetically divergent South American Strains of Toxoplasma gondii. PLoS Genet 11(8):e1005434. https://doi.org/10.1371/journal.pgen.1005434
Bernstein M, Pardini L, Moré G, Unzaga JM, Su C, Venturini MC (2018) Population structure of Toxoplasma gondii in Argentina. Infect Genet Evol 65:72–79. https://doi.org/10.1016/j.meegid.2018.07.018
Bernstein M, Pardini L, Campero LM, Helman E, Unzaga JM, Venturini MC, Moré G (2020) Evaluation of biological behavior of Toxoplasma gondii atypical isolates # 14 and # 163. Exp Parasitol 211:107860. https://doi.org/10.1016/j.exppara.2020.107860
Bernstein, M., Pardini, L., Bello Pede Castro, B., Unzaga, J.M., Venturini, M.C., Moré, G. (2021) ROP18 and ROP5 alleles combinations are related with virulence of T. gondii isolates from Argentina. Parasitol Int, 102328. https://doi.org/10.1016/j.parint.2021.102328.
Blaizot R, Nabet C, Blanchet D, Martin E, Mercier A, Darde ML, Elenga N, Demar M (2019) (2019) Pediatric Amazonian toxoplasmosis caused by atypical strains in French Guiana, 2002–2017. Pediatr Infect Dis J 38(3):e39–e42. https://doi.org/10.1097/INF.0000000000002130
Carneiro AC, Andrade GM, Costa JG, Pinheiro BV, Vasconcelos-Santos DV, Ferreira AM, Su C, Januário JN, Vitor RW (2013) Genetic characterization of Toxoplasma gondii revealed highly diverse genotypes for isolates from newborns with congenital toxoplasmosis in southeastern Brazil. J Clin Microbiol 51(3):901–907. https://doi.org/10.1128/jcm.02502-12
Carral L, Kaufer F, Pardini L, Durlach R, Moré G, Venturini MC, Freuler C (2018) Toxoplasmosis congénita: Diagnóstico serológico, RPC, aislamiento y caracterización molecular de Toxoplasma gondii. Rev Chil Infectol 35(1):36–40. https://doi.org/10.4067/s0716-10182018000100036
De-la-Torre A, Sauer A, Pfaff AW, Bourcier T, Brunet J, Speeg-Schatz C, Ballonzoli L, Villard O, Ajzenberg D, Sundar N, Grigg ME, Gomez-Marin JE, Candolfi E (2013) Severe South American ocular toxoplasmosis is associated with decreased Ifn-γ/Il-17a and increased Il-6/Il-13 intraocular levels. PLoS Negl Trop Dis 7:e2541. https://doi.org/10.1371/journal.pntd.0002541
Dellarupe, A., Fitte, B., Pardini, L., Campero, L. M., Bernstein, M., Robles, M. R., Moré, G., Venturini, M. C., Unzaga, J. M. (2019) Toxoplasma gondii and Neospora caninum infections in synanthropic rodents from Argentina. Rev Bras Parasitol Vet, 28 (1). https://doi.org/10.1590/S1984-29612019009.
Dubey JP (2022) Toxoplasmosis of animals and humans, 3rd edn. CRC Press, Boca Raton, Florida, p 564
Durlach R, Freuler C, Messina M, Freilij H, González Ayala S, Venturini MC, Kaufer F, García F, Ceriotto M, Pardini L, Nadal M, Ortiz De Zárate M, Schneider V, Mayer-Wolf M, Jacob N, Abuin JC, Altcheh J, Fiameni F, Salomon C, Ledesma B, Eduardo E (2021) Consenso Argentino de toxoplasmosis congénita 2020. Medicina (buenos Aires) 81(2):257–268
Ferreira IM, Vidal JE, de Mattos CD, de Mattos LC, Qu D, Su C, Pereira-Chioccola VL (2011) Toxoplasma gondii isolates: multilocus RFLP-PCR genotyping from human patients in Sao Paulo State Brazil Identified Distinct Genotypes. Exp Parasitol 129(2):190–195. https://doi.org/10.1016/j.exppara.2011.06.002
Pardini L, Carral LA, Bernstein M, Gos ML, Olejnik P, Unzaga JM, Kaufer FJ, Freuler CB, Durlach RA, Venturini MC (2014) First isolation and molecular characterization of Toxoplasma gondii from a human placenta in Argentina. Parasitol Int 63(2014):470–472. https://doi.org/10.1016/j.parint.2013.10.011
Pardini L, Bernstein M, Carral LA, Kaufer FJ, Dellarupe A, Gos ML, Campero ML, Moré G, Messina MT, Schneider MV, Freuler CB, Durlach RA, Unzaga JM, Venturini MC (2019) Congenital human toxoplasmosis caused by non-archetypal Toxoplasma gondii genotypes in Argentina. Parasitol Int 68:48–52. https://doi.org/10.1016/j.parint.2018.10.002
Pardini, L., Moré, G., Rudzinski, M., Gos, M.L., Campero, L.M., Meyer, A., Bernstein, M., Unzaga, J.M., Venturini, M.C. (2016) Toxoplasma gondii isolates from chickens in an area with human toxoplasmic retinochoroiditis. Exp Parasitol, pp. 16–20. https://doi.org/10.1016/j.exppara.2016.03.006.
Pena HF, Gennari SM, Dubey JP, Su C (2008) Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int J Parasitol 38:561–569. https://doi.org/10.1016/j.ijpara.2007.09.004
Postma GC, Dellarupe A, Streitenberger N, Bratanich A, Venturini MC, Minatel L (2019) Canine distemper virus, atypical Toxoplasma gondii, and Neospora caninum co-infection, in a dog with neurological signs from Argentina. Braz J Vet Pathol 12(3):101–105. https://doi.org/10.24070/bjvp.1983-0246.v12i3p101-105
Rudzinski M, Meyer A (2011) Prevalence and risk factors associated with ocular toxoplasmosis in patients from the center east region of the province of Misiones Argentina. Oftalmol Clin Exp 4(4):159–162
Saraf P, Shwab EK, Dubey JP, Su C (2017) On the determination of Toxoplasma gondii virulence in mice. Exp Parasitol 174:25–30. https://doi.org/10.1016/j.exppara.2017.01.009
Shwab EK, Jiang T, Pena HFJ, Gennari SM, Dubey JP, Su C (2016) The ROP18 and ROP5 gene allele types are highly predictive of virulence in mice across globally distributed strains of Toxoplasma gondii. Int J Parasitol 46:141–146. https://doi.org/10.1016/j.ijpara.2015.10.005
Su C, Zhang X, Dubey JP (2006) Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int J Parasitol 36:841–848. https://doi.org/10.1016/j.ijpara.2006.03.003
Weiss LM, Kim K (2014) Toxoplasma gondii the model Apicomplexan: perspectives and methods, First Edition. ELSEVIER, Ed., United Kingdom, p 1085
Acknowledgements
We would like to thank Dr. Chunlei Su for providing the T. gondii DNA of reference strains and for his advice in the standardization process of the ROP18/ROP5 nPCR-RFLP technique. Additionally, we would like to thank Mr. Isidoro Ercoli and Mrs. Selva Peñaloza for their technical assistance.
Funding
This work was partially supported by the Fund for Scientific and Technological Research (FONCyT) through PICT 2012–0355 and PICT 2016–3117; La Plata National University I + D project V250 and young researchers grant 1685/18. Mariana Bernstein was awarded a postdoctoral fellowship from National Council for Scientific and Technical Research (CONICET) to fulfill this study.
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M. B.: Investigation; Writing—original draft; Writing—review & editing. M. R.: Resources. V. S.: Resources. M. M.: Resources. M. L. G.: Investigation. E. H.: Formal analysis. A. D.: Investigation. J. M. U.: Funding acquisition; Writing—review & editing. M C. V.: Funding acquisition. G. M.: Conceptualization; Writing—review & editing. L. P.: Conceptualization; Supervision; Writing—review & editing.
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Bernstein, M., Rudzinski, M., Schneider, V. et al. Genetic characterization of Toxoplasma gondii from human and chicken isolates from Argentina. Parasitol Res 123, 129 (2024). https://doi.org/10.1007/s00436-024-08142-z
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DOI: https://doi.org/10.1007/s00436-024-08142-z