Atypical strains of Toxoplasma gondii and its impact on development of toxoplasmosis

Authors

DOI:

https://doi.org/10.33448/rsd-v12i2.39884

Keywords:

Toxoplasma gondii; Genotyping; Toxoplasmosis.

Abstract

This article aims to clarify the population structure of T. gondii strains, their virulence patterns, and the characterization of atypical strains addressing changes and complications related to T. gondii strains. Fifty-nine references in Portuguese, English, and Spanish from 1992 to 2021 were selected from the research bases PubMed, SciELO, Elsevier, ScienceDirect, and Google Scholar, using the keywords Toxoplasma gondii, Genotyping, and toxoplasmosis alone or in a combined form. T. gondii has a life cycle with well-defined sexual reproduction that occurs in nature more rarely in countries of North America and Europe. Based on strains isolated in these regions, the population of T. gondii was differentiated into three clonal lineages, implying a low genetic diversity. Despite the observed genotypic pattern, South America, especially Brazil, has shown the existence of a higher genetic variability, characterizing non-clonal genotype strains called atypical. The presence of these strains may be associated with the wide geographic distribution, fauna, and recombination of clonal strains through the sexual cycle in the feline. The correlation between the virulence of the Brazilian strains and the symptoms presented by patients with toxoplasmosis is not well-defined yet. However, these patients show a greater severity of the disease compared to infections in European and North American countries, pointing to a possible relationship between the genetic polymorphism of T. gondii strains with the pathogenesis of toxoplasmosis.

References

Adl, S. M., Simpson, A. G. B., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., le Gall, L., Lynn, D. H., McManus, H., Mitchell, E. A. D., Mozley-Stanridge, S. E., Parfrey, L. W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C. R., Smirnov, A., & Spiegel, F. W. (2012). The Revised Classification of Eukaryotes. Journal of Eukaryotic Microbiology, 59(5), 429–514. https://doi.org/10.1111/j.1550-7408.2012.00644.x

Ajzenberg, D., Dumetre, A., & Dardé, M. L. (2005). Multiplex PCR for typing strains of Toxoplasma gondii. Journal of clinical microbiology, 43(4), 1940-1943.

Alday, P. H., & Doggett, J. S. (2017). Drugs in development for toxoplasmosis: Advances, challenges, and current status. Drug Design, Development and Therapy, 11, 273–293. https://doi.org/10.2147/DDDT.S60973

Andrade, M. M. C. (2012). Prevalência da toxoplasmose em ovinos e caracterização molecular de isolados de Toxoplasma gondii (Nicolle & Manceaux, 1909) obtidos de animais de produção no Estado do Rio Grande do Norte (Tese). Universidade Federal de Minas Gerais, Belo Horizonte, Brasil.

Artigas, R. S., Amores, W. G., Valdes, D. C., Batista, Y. G., & Cruz, A. M. (2012). Aspectos básicos sobre la patogenia, respuesta inmune y bioseguridad en el trabajo con el Toxoplasma gondii. Correo Científico Médico de Holguín, 16(1). https://www.medigraphic.com/cgi-bin/new/resumen.cgi?IDARTICULO=39301

Aspinall, T. V., Joynson, D. H. M., Guy, E., Hyde, J. E., & Sims, P. F. G. (2002). The molecular basis of sulfonamide resistance in Toxoplasma gondii and implications for the clinical management of toxoplasmosis. The Journal of Infectious Diseases, 185(11), 1637–1643. https://doi.org/10.1086/340577

Aun, F. G. (2019). Toxoplasmose cerebral em pessoas que vivem com HIV/aids: Perfis epidemiológico, clínico, terapêutico e de neuroimagem. https://repositorio.unesp.br/handle/11449/183199

Belfort, R. N., Nussenblatt, V., Rizzo, L., Muccioli, C., Silveira, C., Nussenblatt, R., Khan, A., Sibley, L. D., & Belfort-Jr., R. (2007). High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, Southern Brazil. Anais Da Academia Brasileira de Ciências, 79, 111–114. https://doi.org/10.1590/S0001-37652007000100013

Bernardo, W. M., Nobre, M. R. C., & Jatene, F. B. (2004). A prática clínica baseada em evidências. Parte II: buscando as evidências em fontes de informação. Rev. Assoc. Med. Bras. 50(1). https://www.scielo.br/pdf/ramb/v50n1/a45v50n1.pdf.

Boothroyd, J. C., & Grigg, M. E. (2002). Population biology of Toxoplasma gondii and its relevance to human infection: Do different strains cause different disease? Current Opinion in Microbiology, 5(4), 438–442. https://doi.org/10.1016/S1369-5274(02)00349-1

Brandão, G. P., Ferreira, A. M., Melo, M. N., & Vitor, R. W. A. (2006). Characterization of Toxoplasma gondii from domestic animals from Minas Gerais, Brazil. Parasite, 13(2), Art. 2. https://doi.org/10.1051/parasite/2006132143

Campina, M. T., & Queiroz-Fernandes, G. M. de. (2018). Neurotoxoplasmose em pacientes imunocomprometidos e a relevância do diagnóstico por imagem. Rev. Salusvita (Online), 421–435.

Cañón-Franco, W. A., Araújo, F. A. P., López-Orozco, N., Jardim, M. M. A., Keid, L. B., Dalla-Rosa, C., Cabral, A. D., Pena, H. F. J., & Gennari, S. M. (2013a). Toxoplasma gondii in free-ranging wild small felids from Brazil: molecular detection and genotypic characterization. Veterinary parasitology, 197(3-4), 462-469.

Cañon-Franco, W. A., Araújo, F. A. P. D., & Gennari, S. M. (2013b). Toxoplasma gondii in small neotropical wild felids. Braz J Vet Res Anim Sci, 50(1), 50-67.

Carme, B., Demar, M., Ajzenberg, D., & Dardé, M. L. (2009). Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerging infectious diseases, 15(4), 656.

Carneiro, A. C. A. V., Andrade, G. M., Costa, J. G. L., Pinheiro, B. V., Vasconcelos-Santos, D. V., Ferreira, A. M., Su, C., Januário, J. N., & Vitor, R. W. A. (2013). Genetic Characterization of Toxoplasma gondii Revealed Highly Diverse Genotypes for Isolates from Newborns with Congenital Toxoplasmosis in Southeastern Brazil. Journal of Clinical Microbiology, 51(3), 901–907. https://doi.org/10.1128/JCM.02502-12

Cavalcante, A. C. R., Ferreira, A. M., Melo, M. N., Fux, B., Brandão, G. P., & Vitor, R. W. A. (2007). Virulence and molecular characterization of Toxoplasma gondii isolated from goats in Ceará, Brazil. Small Ruminant Research, 69(1), 79–82. https://doi.org/10.1016/j.smallrumres.2005.12.023

Chorlton, S. D. (2019). Adjunctive bradyzoite-directed therapy for reducing complications of congenital toxoplasmosis. Medical Hypotheses, 133, 109376. https://doi.org/10.1016/j.mehy.2019.109376

Cordeiro, A. M., Oliveira, G. M. D., Rentería, J. M., & Guimarães, C. A. (2007). Revisão sistemática: uma revisão narrativa. Revista do Colégio Brasileiro de Cirurgiões, 34, 428-431.

Cristina, N., Dardé, M. L., Boudin, C., Tavernier, G., Pestre-Alexandre, M., & Ambroise-Thomas, P. (1995). A DNA fingerprinting method for individual characterization ofToxoplasma gondii strains: Combination with isoenzymatic characters for determination of linkage groups. Parasitology Research, 81(1), 32–37. https://doi.org/10.1007/BF00932414

Dardé, M. L., Bouteille, B., & Pestre-Alexandre, M. (1992). Isoenzyme Analysis of 35 Toxoplasma gondii Isolates and the Biological and Epidemiological Implications. The Journal of Parasitology, 78(5), 786–794. https://doi.org/10.2307/3283305

de Lima Bessa, G., de Almeida Vitor, R. W., & dos Santos Martins-Duarte, E. (2021). Toxoplasma gondii in South America: A differentiated pattern of spread, population structure and clinical manifestations. Parasitology Research, 120(9), 3065–3076. https://doi.org/10.1007/s00436-021-07282-w

de Melo Ferreira, A., Vitor, R. W. A., Gazzinelli, R. T., & Melo, M. N. (2006). Genetic analysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR–RFLP. Infection, Genetics and Evolution, 6(1), 22–31. https://doi.org/10.1016/j.meegid.2004.12.004

Dedicoat, M., & Livesley, N. (2006). Management of toxoplasmic encephalitis in HIV‐infected adults (with an emphasis on resource‐poor settings). Cochrane Database of Systematic Reviews, 3. https://doi.org/10.1002/14651858.CD005420.pub2

Delhaes, L., Ajzenberg, D., Sicot, B., Bourgeot, P., Dardé, M.-L., Dei-Cas, E., & Houfflin-Debarge, V. (2010). Severe congenital toxoplasmosis due to a Toxoplasma gondii strain with an atypical genotype: Case report and review. Prenatal Diagnosis, 30(9), 902–905. https://doi.org/10.1002/pd.2563

Dubey, J. P. (2008). The History of Toxoplasma gondii—The First 100 Years. Journal of Eukaryotic Microbiology, 55(6), 467–475. https://doi.org/10.1111/j.1550-7408.2008.00345.x

Dubey, J. P., Gennari, S. M., Sundar, N., Vianna, M. C. B., Bandini, L. M., Yai, L. E. O., Kwok, O. C. H., & Su, C. (2007). Diverse and atypical genotypes identified in Toxoplasma gondii from dogs in São Paulo, Brazil. Journal of Parasitology, 93(1), 60–64. https://doi.org/10.1645/GE-972R.1

Dubey, J. P., Lindsay, D. S., & Speer, C. A. (1998). Structures of Toxoplasma gondiiTachyzoites, Bradyzoites, and Sporozoites and Biology and Development of Tissue Cysts. Clinical Microbiology Reviews, 11(2), 267–299. https://doi.org/10.1128/CMR.11.2.267

Dubey, J. P. (2010). Diagnosis. In: Toxoplasmoses of animals and humans. CRC Press, 52-71.

Ercole, F. F., Melo, L. S., & Alcoforado, C. L. G. C. (2014). Revisão integrativa versus revisão sistemática. Reme: Revista Mineira de Enfermagem, 18(1), 09–11. https://doi.org/10.5935/1415-2762.20140001

Ferreira, A. M., Martins, M. S., & Vitor, R. W. A. (2001). Virulence for BALB/c mice and antigenic diversity of eight Toxoplasma gondii strains isolated from animals and humans in Brazil. Parasite, 8(2), 99-105.

Frazão-Teixeira, E., Sundar, N., Dubey, J. P., Grigg, M. E., & de Oliveira, F. C. R. (2011). Multi-locus DNA sequencing of Toxoplasma gondii isolated from Brazilian pigs identifies genetically divergent strains. Veterinary Parasitology, 175(1), 33–39. https://doi.org/10.1016/j.vetpar.2010.09.030

Gilbert, R. E., Freeman, K., Lago, E. G., Bahia-Oliveira, L. M., Tan, H. K., Wallon, M., Buffolano, W., Stanford, M. R., Petersen E., & European Multicentre Study on Congenital Toxoplasmosis (EMSCOT). (2008). Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Neglected Tropical Diseases, 2(8), e277.

Gómez, A. S., Quaranta, A. M., Pirota, M. F., & Quaranta, D. T. R. (2007). TOXOPLASMOSIS: SUS FORMAS CLINICAS. 5.

Gómez-Marín, J. E. (2010). Toxoplasmose congênita em crianças sul-americanas: [Revisão]. Sci. med. http://revistaseletronicas.pucrs.br/ojs/index.php/scientiamedica/article/view/5504/5064

Howe, D. K., & Sibley, L. D. (1995). Toxoplasma gondii Comprises Three Clonal Lineages: Correlation of Parasite Genotype with Human Disease. The Journal of Infectious Diseases, 172(6), 1561–1566. https://doi.org/10.1093/infdis/172.6.1561

Khan, A., Jordan, C., Muccioli, C., Vallochi, A. L., Rizzo, L. V., Belfort, R., Vitor, R. W. A., Silveira, C., & Sibley, L. D. (2006). Genetic Divergence of Toxoplasma gondii Strains Associated with Ocular Toxoplasmosis, Brazil. Emerging Infectious Diseases, 12(6), 942–949. https://doi.org/10.3201/eid1206.060025

Kieffer, F., & Wallon, M. (2013). Chapter 112—Congenital toxoplasmosis. Em O. Dulac, M. Lassonde, & H. B. Sarnat (Orgs.), Handbook of Clinical Neurology (Vol. 112, p. 1099–1101). Elsevier. https://doi.org/10.1016/B978-0-444-52910-7.00028-3

Lopes, C. C. H., & Berto, B. P. (2012). Aspectos associados à toxoplasmose: Uma referência aos principais surtos no Brasil. Saúde & Ambiente em Revista, 7(2), Art. 2.

Maldonado, Y. A., Read, J. S., & Committee On Infectious Diseases. (2017). Diagnosis, Treatment, and Prevention of Congenital Toxoplasmosis in the United States. Pediatrics, 139(2), e20163860. https://doi.org/10.1542/peds.2016-3860

Marzola, P. E. R. (2021). Incidência de toxoplasmose congênita e fatores associados em um hospital no sul do Brasil. https://repositorio.animaeducacao.com.br/handle/ANIMA/13015

Medeiros, L. C. (2019). Interação de Toxoplasma gondii e células epiteliais intestinais de felinos in vitro. https://www.arca.fiocruz.br/handle/icict/39501

Melo, L. M. C. de, Paulista, M. T., & Sánchez, T. E. G. (2020). Neurotoxoplasmose em pacientes portadores de Imunodeficiência Humana e suas sequelas: Uma revisão narrativa / Neurotoxoplasmosis in patients with Human Immunodeficiency and its sequelae: A narrative review. Brazilian Journal of Development, 6(10), 81527–81538. https://doi.org/10.34117/bjdv6n10-542

Montazeri, M., Mehrzadi, S., Sharif, M., Sarvi, S., Tanzifi, A., Aghayan, S. A., & Daryani, A. (2018). Drug Resistance in Toxoplasma gondii. Frontiers in Microbiology, 9, 2587. https://doi.org/10.3389/fmicb.2018.02587

Monteiro, A. C. B., Iano, Y., França, R. P., & Arthur, R. (2019). Toxoplasmosis Gondii: From Discovery to Advancens in Image Processing. Em Y. Iano, R. Arthur, O. Saotome, V. Vieira Estrela, & H. J. Loschi (Orgs.), Proceedings of the 4th Brazilian Technology Symposium (BTSym’18) (p. 91–101). Springer International Publishing. https://doi.org/10.1007/978-3-030-16053-1_9

Mota de Sousa, L. M., Furtado Firmino, C., Alves Marques-Vieira, C. M., Silva Pedro Severino, S., & Castelão Figueira Carlos Pestana, H. (2018). Revisões da literatura científica: Tipos, métodos e aplicações em enfermagem. Revista Portuguesa de Enfermagem de Reabilitação, 1(1), 45–55. https://doi.org/10.33194/rper.2018.v1.n1.07.4391

Pena, H. F. J., Gennari, S. M., Dubey, J. P., & Su, C. (2008). Population structure and mouse-virulence of Toxoplasma gondii in Brazil. International Journal for Parasitology, 38(5), 561–569. https://doi.org/10.1016/j.ijpara.2007.09.004

Ribeiro, J. L. P. (2014). Revisão de investigação e evidência cientifica. Revista Sociedade Portuguesa de Psicologia da Saúde, 15(3)

Rorman, E., Zamir, C. S., Rilkis, I., & Ben-David, H. (2006). Congenital toxoplasmosis—Prenatal aspects of Toxoplasma gondii infection. Reproductive Toxicology, 21(4), 458–472. https://doi.org/10.1016/j.reprotox.2005.10.006

Santos, R. A., Rocha, I. T. M., & Ramos, R. (2015). Toxoplasmose em pacientes imunocomprometidos: Aspectos epidemiológicos e clínicos. Bol. epidemiol. (Porto Alegre, Online), 3–8.

Shwab, E. K., Zhu, X.-Q., Majumdar, D., Pena, H. F. J., Gennari, S. M., Dubey, J. P., & Su, C. (2014). Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology, 141(4), 453–461. https://doi.org/10.1017/S0031182013001844

Sibley, L. D., Mordue, D., & Howe, D. K. (1999). Experimental Approaches to Understanding Virulence in Toxoplasmosis. Immunobiology, 201(2), 210–224. https://doi.org/10.1016/S0171-2985(99)80061-8

Silva, L. A., Andrade, R. O., Carneiro, A. C. A. V., & Vitor, R. W. A. (2014). Overlapping Toxoplasma gondii Genotypes Circulating in Domestic Animals and Humans in Southeastern Brazil. PLOS ONE, 9(2), e90237. https://doi.org/10.1371/journal.pone.0090237

Su, C., Zhang, X., & Dubey, J. P. (2006). Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. International journal for parasitology, 36(7), 841-848.

Torres-Castro, M., Muñoz-Dueñas, D., Hernández-Betancourt, S., Bolio-González, M., Noh-Pech, H., Peláez-Sánchez, R., & Sosa-Escalante, J. (2019). Infección con Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) en murciélagos de Campeche y Yucatán, México. Revista de Biología Tropical, 67(3), 633–642. https://doi.org/10.15517/rbt.v67i3.35147

Valladares, B. T. N., Sánchez, M. A. L., Rojas, M. B. I., & Padrón, L. S. (2020). Toxoplasmosis ocular: aspectos clínico-epidemiológicos en edad pediátrica. Revista de Ciencias Médicas de Pinar del Río, 24(4).

Vommaro, R. C., Martins-Duarte, É. S., & de Souza, W. (2014). Quimioterapia Experimental. Toxoplasmose & Toxoplasma gondii, 99.

Walcher, D. L., Comparsi, B., & Pedroso, D. (2017). Toxoplasmose gestacional: Uma revisão. Rev. bras. anal. clin, 323–327.

Wallon, M., & Peyron, F. (2018). Congenital Toxoplasmosis: A Plea for a Neglected Disease. Pathogens, 7(1), Art. 1. https://doi.org/10.3390/pathogens7010025

Published

14/01/2023

How to Cite

VIEIRA, G. C. D. .; DUARTE, Érica dos S. M. . Atypical strains of Toxoplasma gondii and its impact on development of toxoplasmosis. Research, Society and Development, [S. l.], v. 12, n. 2, p. e3412239884, 2023. DOI: 10.33448/rsd-v12i2.39884. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/39884. Acesso em: 20 apr. 2024.

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Review Article