Abstract
Toxoplasma gondii is an obligate intracellular parasite belonging to the phylum Apicomplexa. It has a worldwide distribution and can infect a wide variety of intermediate hosts, including humans. In South America, toxoplasmosis shows high health impacts, and the incidence of the disease is frequently reported and more severe than in other regions, such as Europe. Although most T. gondii infections are asymptomatic, severe manifestations can occur in cases of congenital toxoplasmosis and immunocompromised individuals. In South America, the ocular disease in immunocompetent individuals is also frequently reported. Treatment for any clinical manifestation of toxoplasmosis consists of the combination of sulfadiazine (SDZ) and pyrimethamine (PYR). However, failures in the treatment of toxoplasmosis have been reported, especially in South America, suggesting the acquisition of resistance against SDZ and PYR. Another paradigm present in the literature is that once infected with T. gondii, the host is immunologically protected from further reinfections. However, some studies indicate cases of congenital transmission of T. gondii from immunocompetent pregnant women with chronic infection, suggesting the possibility of reinfection in humans. Thus, in this review, we will cover several aspects of South American T. gondii isolates, such as genetic characterization, disease manifestation, host reinfection and drug resistance.
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Aloise DA, Wendel Coura-Vital W, Carneiro M, Rodrigues MV, Toscano GAS, Silva RB, Silva-Portela RCB, Fontes-Dantas FL, Agnez-Lima LF, Vitor RWA, Andrade Neto VF (2021) Association between ocular toxoplasmosis and APEX1 and MYD88 polymorphism. Acta Trop 9:106006. https://doi.org/10.1016/j.actatropica.2021.106006
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 186:684–689. https://doi.org/10.1086/342663
Álvarez Barreneche MF, Restrepo Castro CA, Hidrón Botero A, Villa Franco JP, Trompa Romero IM, Restrepo Carvajal L, Eusse García A, Ocampo Mesa A, Echeverri Toro LM, Fernández P, de Castro GP, Ramírez Rivera JM, Agudelo Restrepo CA (2017) Hospitalization causes and outcomes in HIV patients in the late antiretroviral era in Colombia. AIDS Res Ther 14:60. https://doi.org/10.1186/s12981-017-0186-3
Alves CF, Vitor RWA (2005) Efficacy of Atovaquone and Sulfadiazine in the Treatment of Mice Infected with Toxoplasma gondii Strains Isolated in Brazil. Parasite 12:171–177. https://doi.org/10.1051/parasite/2005122171
Aspinall TV, Joynson DH, Guy E, Hyde JE, Sims PF (2002) The molecular basis of sulfonamide resistance in Toxoplasma gondii and implications for the clinical management of toxoplasmosis. J Infect Dis 185:1637–1643. https://doi.org/10.1086/340577
Belfort-Neto R, Nussenblatt V, Rizzo L, Muccioli C, Silveira C, Nussenblatt R, Khan A, Sibley LD, Belfort R Jr (2007) High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim Southern Brazil. An Acad Bras Cienc 79:111–114. https://doi.org/10.1590/s0001-37652007000100013
Bessa GL, Costa JGL, Rêgo WMF, Baraviera RCA, Pinto LV, Lopes REN, Vitor RWA (2019) Tissue Dissemination and Humoral Response after Experimental Reinfection with Atypical Toxoplasma gondii Strains Obtained from Congenital Human Toxoplasmosis in Brazil. Exp Parasitol 207:107781. https://doi.org/10.1016/j.exppara.2019.107781
Bigna JJ, Tochie JN, Tounouga DN, Bekolo AO, Ymele NS, Youda EL, Sime PS, Nansseu JR (2020) Global, Regional, and Country Seroprevalence of Toxoplasma gondii in Pregnant Women: A Systematic Review. Modelling and Meta-Analysis Sci Rep 10:12102. https://doi.org/10.1038/s41598-020-69078-9
Blaizot R, Nabet C, Laghoe L, Faivre B, Escotte-Binet S, Djossou F, Mosnier E, Henaff F, Blanchet D, Mercier A, Dardé ML, Villena I, Demar M (2020) Outbreak of Amazonian Toxoplasmosis: A One Health Investigation in a Remote Amerindian Community. Front Cell Infect Microbiol 10:401. https://doi.org/10.3389/fcimb.2020.00401
Bosch-Driessen LH, Verbraak FD, Suttorp-Schulten MS, van Ruyven RL, Klok AM, Hoyng CB, Rothova A (2002) A prospective, randomized trial of pyrimethamine and azithromycin vs pyrimethamine and sulfadiazine for the treatment of ocular toxoplasmosis. Am J Ophthalmol 134:34–40. https://doi.org/10.1016/S0002-9394(02)01537-4
Bossi P, Caumes E, Paris L, Dardé ML, Bricaire F (1998) Toxoplasma gondii-associated Guillain-Barré syndrome in an immunocompetent patient. J Clin Microbiol 36:3724–3725. https://doi.org/10.1128/jcm.36.12.3724-3725.1998
Brandão-de-Resende C, Santos HH, Rojas Lagos AA, Lara CM, Arruda JSD, Marino APMP, do Valle Antonelli LR, Gazzinelli RT, de Almeida Vitor RW, Vasconcelos-Santos DV, (2020) Clinical and Multimodal Imaging Findings and Risk Factors for Ocular Involvement in a Presumed Waterborne Toxoplasmosis Outbreak, Brazil1. Emerg Infect Dis 26:2922–2932. https://doi.org/10.3201/EID2612.200227
Brandão GP, Melo MN, Caetano BC, Carneiro CM, Silva LA, Vitor RW (2011) Susceptibility to re-infection in C57BL/6 mice with recombinant strains of Toxoplasma gondii. Exp Parasitol 128(4):433–437. https://doi.org/10.1016/j.exppara.2011.05.015
Carme B, Demar M, Ajzenberg D, Dardé ML (2009) Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg Infect Dis 15:656–658. https://doi.org/10.3201/eid1504.081306
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 51:901–907. https://doi.org/10.1128/JCM.02502-12
Carneiro AC, Machado AS, Béla SR, Costa JG, Andrade GM, Vasconcelos-Santos DV, Januário JN, Coelho-Dos-Reis JG, Ferro EA, Teixeira-Carvalho A, Vitor RW, Martins-Filho OA, UFMG Congenital Toxoplasmosis Brazilian Group (2016) Cytokine signatures associated with early onset, active lesions and late cicatricial events of retinochoroidal commitment in infants with congenital toxoplasmosis. J Infect Dis 213:1962–70. https://doi.org/10.1093/infdis/jiw041
Chiappe Gonzalez AJ, Vargas Matos I, Massucco Revoredo V (2020) Acute toxoplasmosis complicated with myopericarditis and possible encephalitis in an immunocompetent patient. Idcases 20:e00772. https://doi.org/10.1016/j.idcr.2020.e00772
Coelho L, Cardoso SW, Amancio RT, Moreira RI, Campos DP, Veloso VG, Grinsztejn B, Luz PM (2014) Trends in AIDS-defining opportunistic illnesses incidence over 25 years in Rio de Janeiro. Brazil Plos One 9:e98666. https://doi.org/10.1371/journal.pone.0098666
Cortés DA, Aguilar MC, Ríos HA, Rodríguez FJ, Montes KV, Gómez-Marín JE, De la Torre A (2020) Severe acute multi-systemic failure with bilateral ocular toxoplasmosis in immunocompetent patients from urban settings in Colombia: Case reports. Am J Ophthalmol Case Rep 18:100661. https://doi.org/10.1016/j.ajoc.2020.100661
Cortés LJ, Duque S, López MC, Moncada D, Molina D, Gómez-Marín JE, Gunturiz ML (2014) Polimorfismos en los genes de dihidrofolato-reductasa ( dhfr ) y dihidropteroato-sintasa ( dhps ) y modelado estructural del gen dhps en aislamientos colombianos de Toxoplasma gondii [Gene polymorphisms in the dihydrofolate reductase ( dhfr ) and dihydropteroate synthase ( dhps ) genes and structural modelling of the dhps gene in Colombian isolates of Toxoplasma gondii]. Biomedica 34:556–566. https://doi.org/10.7705/biomedica.v34i4.2132
Costa JGL, Tavares AT, Silva DRC, Pinto LV, Baraviera RCA, Noviello MLM, Arantes RME, Vitor RWA (2018) Kinetics of parasite distribution after reinfection with genetically distinct strains of Toxoplasma gondii. Exp Parasitol 184:22–30. https://doi.org/10.1016/j.exppara.2017.11.003
Caribbean, Central and South America Network for HIV Epidemiology (CCASAnet), of the International Epidemiologic Databases to Evaluate AIDS (IeDEA) Program (2016) Time to HAART Initiation after Diagnosis and Treatment of Opportunistic Infections in Patients with AIDS in Latin America. PLoS One 11:e0153921. https://doi.org/10.1371/journal.pone.0153921.
Dardé ML, Villena I, Pinon JM, Beguinot I (1998) Severe toxoplasmosis caused by a Toxoplasma gondii strain with a new isoenzyme type acquired in French Guyana. J Clin Microbiol 36:324. https://doi.org/10.1128/jcm.36.1.324-324.1998
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.
de-la-Torre A, Gómez-Marín J (2020) Disease of the Year 2019: Ocular Toxoplasmosis in HIV-infected Patients. Ocul Immunol Inflamm 28(7):1031-1039. https://doi.org/10.1080/09273948.2020.1735450
de-la-Torre A, Pfaff WA, Grigg ME, Villard O, Candolfi E, Gomez-Marin JE (2014) Ocular Cytokinome Is Linked to Clinical Characteristics in Ocular Toxoplasmosis. Cytokine 68, 1: 23–31. https://doi.org/10.1016/j.cyto.2014.03.005.
Demar M, Ajzenberg D, Maubon D, Djossou F, Panchoe D, Punwasi W, Valery N, Peneau C, Daigre JL, Aznar C, Cottrelle B, Terzan L, Dardé ML, Carme B (2007) Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clin Infect Dis 45:e88-95. https://doi.org/10.1086/521246
Dubey JP (2008) The history of Toxoplasma gondii–the first 100 years. J Eukaryot Microbiol 55:467–475. https://doi.org/10.1111/j.1550-7408.2008.00345.x
Dubey JP (2010) Toxoplasmosis of Animals and Humans, 2nd edn. CRC Press Inc, Boca Raton, FL, USA
Dubey JP, Lago EG, Gennari SM, Su C, Jones JL (2012) Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139:1375–1424. https://doi.org/10.1017/S0031182012000765
Elbez-Rubinstein A, Ajzenberg D, Dardé ML, Cohen R, Dumètre A, Yera H, Gondon E, Janaud JC, Thulliez P (2009) Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. J Infect Dis 199:280–285. https://doi.org/10.1086/595793
Eyles DE, Coleman N (1953) Synergistic effect of sulfadiazine and daraprim against experimental toxoplasmosis in the mouse. Antibiot Chemother (northfield) 3:483–490
Fernandes SM, Dias AR, Miranda-Scippa  (2020) Association between exposure to toxoplasmosis and major psychiatric disorders: a systematic review. Braz J Psychiatry 18:S1516-44462020005030200. https://doi.org/10.1590/1516-4446-2020-0904
Ferreira Ade M, Vitor RW, Gazzinelli RT, Melo MN (2006) Genetic analysis of natural recombinant Brazilian Toxoplasma gondii strains by multilocus PCR-RFLP. Infect Genet Evol 6:22–31. https://doi.org/10.1016/j.meegid.2004.12.004
Ferreira IM, Vidal JE, Costa-Silva TA, Meira CS, Hiramoto RM, Penalva de Oliveira AC, Pereira-Chioccola VL (2008) Toxoplasma gondii: genotyping of strains from Brazilian AIDS patients with cerebral toxoplasmosis by multilocus PCR-RFLP markers. Exp Parasitol. 118:221e227. https://doi.org/10.1016/j.exppara.2007.08.006
Ferreira IM, Vidal EJ, Mattos CB, 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 129:190–195. https://doi.org/10.1016/j.exppara.2011.06.002
Filisetti D, Candolfi E (2004) Immune response to Toxoplasma gondii. Ann Ist Super Sanita 40(1):71–80. https://doi.org/10.1111/j.1348-0421.1983.tb00604.x
Fortier B, Aïssi E, Ajana F, Dieusart P, Denis P, Martin de Lassalle E, Lecomte-Houcke M, Vinatier D (1991) Spontaneous abortion and reinfection by Toxoplasma gondii. Lancet 338:444. https://doi.org/10.1016/0140-6736(91)91064-2
Franco PS, da Silva NM, de Freitas BB, de Oliveira GA, Ietta F, Shwab EK, Su C, Mineo JR, Ferro EA (2015) Calomys callosus chronically infected by Toxoplasma gondii clonal type II strain and reinfected by Brazilian strains is not able to prevent vertical transmission. Front Microbiol 6:181. https://doi.org/10.3389/fmicb.2015.00181
Franco PS, Gois PSG, de Araújo TE, da Silva RJ, de Freitas BB, de Oliveira GA, Ietta F, Dos Santos LA, Dos Santos MC, Mineo JR, Ferro EAV (2019) Brazilian strains of Toxoplasma gondii are controlled by azithromycin and modulate cytokine production in human placental explants. J Biomed Sci 26:10. https://doi.org/10.1186/s12929-019-0503-3
Gavinet MF, Robert F, Firtion G, Delouvrier E, Hennequin C, Maurin JR, Tourte-Schaefer C, Dupouy-Camet J (1997) Congenital toxoplasmosis due to maternal reinfection during pregnancy. J Clin Microbiol 35:1276–1277. https://doi.org/10.1128/jcm.35.5.1276-1277.1997
Gilbert R (2009) Treatment for congenital toxoplasmosis: finding out what works. Mem Inst Oswaldo Cruz 104:305–311. https://doi.org/10.1590/S0074-02762009000200026
Gilbert RE, Freeman K, Lago EG, Bahia-Oliveira LM, Tan HK, Wallon M, Buffolano W, Stanford MR, Petersen E; European Multicentre Study on Congenital Toxoplasmosis (EMSCOT) (2008) Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Negl Trop Dis. 2(8):e277. https://doi.org/10.1371/journal.pntd.0000277.
Giugno S, Monteleone MM, Insalaco G, Leanza G, Palumbo M, Leanza V (2020) Congenital toxoplasmotic chorioretinitis following reinfection. Eur J Obstet Gynecol Reprod Biol 251:263–265. https://doi.org/10.1016/j.ejogrb.2020.04.045
Glasner PD, Silveira C, Kruszon-Moran D, Martins MC, Burnier Júnior M, Silveira S, Camargo ME, Nussenblatt RB, Kaslow RA, Belfort Júnior R (1992) An unusually high prevalence of ocular toxoplasmosis in southern Brazil. Am J Ophthalmol 114(2):136–144. https://doi.org/10.1016/S0002-9394(14)73976-5
Gómez-Chávez F, Cañedo-Solares I, Ortiz-Alegría LB, Flores-García Y, Figueroa-Damián R, Luna-Pastén H, Gómez-Toscano V, López-Candiani C, Arce-Estrada GE, Bonilla-Ríos CA, Mora-González JC, García-Ruiz R, Correa D (2020) A Proinflammatory Immune Response Might Determine Toxoplasma gondii Vertical Transmission and Severity of Clinical Features in Congenitally Infected Newborns. Front Immunol 11:390. https://doi.org/10.3389/fimmu.2020.00390
Gómez-Marín JE (2010) Congenital toxoplasmosis in South American children. Scientia Medica 20:103–107. https://revistaseletronicas.pucrs.br/ojs/index.php/scientiamedica/article/view/5504
Gómez-Marín JE (2005) Evaluación Del Tratamiento de La Toxoplasmosis Gestacional En Una Cohorte Colombiana. Infectio 9:16. https://www.revistainfectio.org/index.php/infectio/article/view/226/246
Ibrahim Ali M, Abdel Gawad Mousa Ismail M, Abd-Elftah Abd-Allah G, Abdel-Latif M, Mohamed Shaapan R, Salah H, Sayed Abdel Gawad S, Abu-Sarea EY 2020 Toxoplasmosis in Schizophrenic Patients: Immune-diagnosis and Serum Dopamine Level. Pak J Biol Sci. 23:1131-1137. https://doi.org/10.3923/pjbs.2020.1131.1137
Greigert V, Bittich-Fahmi F, Pfaff AW (2020) Pathophysiology of ocular toxoplasmosis: Facts and open questions. PLoS Negl Trop Dis 14(12):e0008905. https://doi.org/10.1371/journal.pntd.0008905
Hill D, Dubey JP (2002) Toxoplasma gondii: transmission, diagnosis and prevention. Clin Microbiol Infect 8(10):634–640. https://doi.org/10.1046/j.1469-0691.2002.00485.x
Holland GN (2009) Ocular toxoplasmosis: the influence of patient age. Mem Inst Oswaldo Cruz 104(2):351–357. https://doi.org/10.1590/S0074-02762009000200031
Hosseini SA, Amouei A, Sharif M, Sarvi S, Galal L, Javidnia J, Pagheh AS, Gholami S, Mizani A, Daryani A (2018) Human toxoplasmosis: a systematic review for genetic diversity of Toxoplasma gondii in clinical samples. Epidemiol Infect 147:1–9. https://doi.org/10.1017/S0950268818002947
Howe DK, Sibley LD (1995) Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis 172(6):1561–1566. https://doi.org/10.1093/infdis/172.6.1561
Jamieson SE, Peixoto-Rangel AL, Hargrave AC, Roubaix LA, Mui EJ, Boulter NR, Miller EN, Fuller SJ, Wiley JS, Castellucci L, Boyer K, Peixe RG, Kirisits MJ, Elias Lde S, Coyne JJ, Correa-Oliveira R, Sautter M, Smith NC, Lees MP, Swisher CN, Heydemann P, Noble AG, Patel D, Bardo D, Burrowes D, McLone D, Roizen N, Withers S, Bahia-Oliveira LM, McLeod R, Blackwell JM (2010) Evidence for associations between the purinergic receptor P2X(7) (P2RX7) and toxoplasmosis. Genes Immun 11(5):374–383. https://doi.org/10.1038/gene.2010.31
Jones JL, Muccioli C, Belfort R Jr, Holland GN, Roberts JM, Silveira C (2006) Recently acquired Toxoplasma gondii infection. Brazil Emerg Infect Dis 12(4):582–587. https://doi.org/10.3201/eid1204.051081
Kiderlen TR, Liesenfeld O, Schürmann D, Schneider T (2011) Toxoplasmic encephalitis in AIDS-patients before and after the introduction of highly active antiretroviral therapy (HAART). Eur J Clin Microbiol Infect Dis 30(12):1521–1525. https://doi.org/10.1007/s10096-011-1254-6
Lau YL, Lee WC, Gudimella R, Zhang G, Ching XT, Razali R, Aziz F, Anwar A, Fong MY (2016) Deciphering the Draft Genome of Toxoplasma gondii RH Strain. PLoS ONE 11(6):e0157901. https://doi.org/10.1371/journal.pone.0157901
Lebas F, Ducrocq S, Mucignat V, Paris L, Mégier P, Baudon JJ, Gold F (2004) Toxoplasmose congénitale: un nouveau cas d’infection pendant la grossesse chez une femme antérieurement immunisée et immunocompétente [Congenital toxoplasmosis: a new case of infection during pregnancy in an previously immunized and immunocompetent woman]. Arch Pediatr 11(8):926–928. https://doi.org/10.1016/j.arcped.2004.04.017
Levine, ND (1988) The Protozoan Phylum Apicomplexa. The Protozoan Phylum Apicomplexa. Vol. 2. CRC Press, USA. https://doi.org/10.1201/9781351076111.
Lindsay DS, Dubey JP (2011) Toxoplasma gondii: the changing paradigm of congenital toxoplasmosis. Parasitology 138(14):1829–1831. https://doi.org/10.1017/S0031182011001478
Lopes FM, Gonçalves DD, Mitsuka-Breganó R, Freire RL, Navarro IT (2007) Toxoplasma gondii infection in pregnancy. Braz J Infect Dis 11(5):496–506. https://doi.org/10.1590/S1413-86702007000500011
Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15(2):211–222. https://doi.org/10.1093/clinids/15.2.211
Machado AS, Carneiro AC, Béla SR, Andrade GM, Vasconcelos-Santos DV, Januário JN, Coelho-dos-Reis JG, Ferro EA, Teixeira-Carvalho A, Vitor RW, Martins-Filho OA, Ufmg Congenital Toxoplasmosis Brazilian Group -UFMG-CTBG (2014) Biomarker analysis revealed distinct profiles of innate and adaptive immunity in infants with ocular lesions of congenital toxoplasmosis. Mediators Inflamm 2014:910621. https://doi.org/10.1155/2014/910621
Mantilla-Muriel LE, Hernández-de-Los-Ríos A, Rincón M, de-la-Torre A, Murillo-León M, Cardona N, Cesbron-Delauw MF, Mercier C, et al (2020) Serotyping, host genes and cytokines response in human ocular toxoplasmosis. Microb Pathog 148:104465. https://doi.org/10.1016/j.micpath.2020.104465.
Meneceur P, Bouldouyre MA, Aubert D, Villena I, Menotti J, Sauvage V, Garin JF, Derouin F (2008) In vitro susceptibility of various genotypic strains of Toxoplasma gondii to pyrimethamine, sulfadiazine, and atovaquone. Antimicrob Agents Chemother 52(4):1269–1277. https://doi.org/10.1128/AAC.01203-07
Montazeri M, Mehrzadi S, Sharif M, Sarvi S, Tanzifi A, Aghayan SA, Daryani A (2018) Drug Resistance in Toxoplasma gondii. Front Microbiol 9:2587. https://doi.org/10.3389/fmicb.2018.02587
Montoya JG, Liesenfeld O (2004) Toxoplasmosis Lancet 363:965–976. https://doi.org/10.1016/S0140-6736(04)16412-X
Montoya JG, Remington JS (2008) Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis 47(4):554–566. https://doi.org/10.1086/590149
Naranjo-Galvis CA, de-la-Torre A, Mantilla-Muriel LE, Beltrán-Angarita L, Elcoroaristizabal-Martín X, McLeod R, Alliey-Rodriguez N, Begeman IJ, López de Mesa C, Gómez-Marín JE, Sepúlveda-Arias JC (2018) Genetic Polymorphisms in Cytokine Genes in Colombian Patients with Ocular Toxoplasmosis. Infect Immun. 86(4): e00597-17. doi: https://doi.org/10.1128/IAI.00597-17.
Nicolle C, Manceaux L (1908) “Sur Une Infection a Corps de Leishman (on Organismes Voisons) Du Gondi.” C R Acad Sci 147: 736–66. http://ci.nii.ac.jp/naid/20000783238/en/.
Pardini L, Bernstein M, Carral LA, Kaufer FJ, Dellarupe A, Gos ML, Campero LM, Moré G, Messina MT, Schneider MV, Freuler CB, Durlach RA, Unzaga JM, Venturini MC (2019) Congenital human toxoplasmosis caused by non-clonal Toxoplasma gondii genotypes in Argentina. Parasitol Int 68(1):48–52. https://doi.org/10.1016/j.parint.2018.10.002
Peixoto-Rangel AL, Miller EN, Castellucci L, Jamieson SE, Peixe RG et al (2009) Candidate gene analysis of ocular toxoplasmosis in Brazil: evidence for a role for toll-like receptor 9 (TLR9). Mem Inst Oswaldo Cruz 104:1187–1190
Pena HF, Gennari SM, Dubey JP, Su C (2008) Population structure and mouse-virulence of Toxoplasma gondii in Brazil. Int J Parasitol 38(5):561–569. https://doi.org/10.1016/j.ijpara.2007.09.004
Petersen E (2007) Prevention and treatment of congenital toxoplasmosis. Expert Rev Anti Infect Ther 5(2):285–293. https://doi.org/10.1586/14787210.5.2.285
Pino LE, Salinas JE, López MC (2009) Descripción de Un Brote Epidémico de Toxoplasmosis Aguda En Pacientes Inmunocompetentes Miembros de Las Fuerzas Militares de Colombia Durante Operaciones de Selva. Infectio 13:83–91. https://doi.org/10.1016/s0123-9392(09)70729-5
Portela RW, Bethony J, Costa MI, Gazzinelli A, Vitor RW, Hermeto FM, Correa-Oliveira R, Gazzinelli RT (2004) A multihousehold study reveals a positive correlation between age, severity of ocular toxoplasmosis, and levels of glycoinositolphospholipid-specific immunoglobulin A. J Infect Dis 190(1):175–183. https://doi.org/10.1086/421505
Rêgo WMF, Costa JGL, Baraviera RCA, Pinto LV, Bessa GL, Lopes REN, Silveira JAG, Vitor RWA (2018) Genetic diversity of Toxoplasma gondii isolates obtained from free-living wild birds rescued in Southeastern Brazil. Int J Parasitol Parasites Wildl 7(3):432–438. https://doi.org/10.1016/j.ijppaw.2018.11.001
Rêgo WMF, Costa JGL, Baraviera RCA, Pinto LV, Bessa GL, Lopes REN, Vitor RWA (2017) Association of ROP18 and ROP5 was efficient as a marker of virulence in atypical isolates of Toxoplasma gondii obtained from pigs and goats in Piauí, Brazil. Vet Parasitol 247:19–25. https://doi.org/10.1016/j.vetpar.2017.09.015
Sánchez V, De-la-Torre A, Gómez-Marín JE (2014) Characterization of ROP18 Alleles in Human Toxoplasmosis. Parasitol Int 63(2):463–469. https://doi.org/10.1016/j.parint.2013.10.012
Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, 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
Shwab EK, Jiang T, Pena HF, 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(2):141–146. https://doi.org/10.1016/j.ijpara.2015.10.005
Shwab EK, Saraf P, Zhu XQ, Zhou DH, McFerrin BM, Ajzenberg D, Schares G, Hammond-Aryee K, van Helden P, Higgins SA, Gerhold RW, Rosenthal BM, Zhao X, Dubey JP, Su C (2018) Human impact on the diversity and virulence of the ubiquitous zoonotic parasite Toxoplasma gondii. Proc Natl Acad Sci U S A 115(29):E6956–E6963. https://doi.org/10.1073/pnas.1722202115
Silva LA, Andrade RO, Carneiro AC, Vitor RW (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
Silva LA, Fernandes MD, Machado AS, Reis-Cunha JL, Bartholomeu DC, Almeida Vitor RW (2019) Efficacy of sulfadiazine and pyrimetamine for treatment of experimental toxoplasmosis with strains obtained from human cases of congenital disease in Brazil. Exp Parasitol 202:7–14. https://doi.org/10.1016/j.exppara.2019.05.001
Silva LA, Reis-Cunha JL, Bartholomeu DC, Vítor RW (2017) Genetic Polymorphisms and Phenotypic Profiles of Sulfadiazine-Resistant and Sensitive Toxoplasma gondii Isolates Obtained from Newborns with Congenital Toxoplasmosis in Minas Gerais. Brazil Plos One 12(1):e0170689. https://doi.org/10.1371/journal.pone.0170689
Silveira C, Ferreira R, Muccioli C, Nussenblatt R, Belfort R (2003) Toxoplamosis Transmitted to a Newborn from the Mother Infected 20 Years Earlier. Am J Ophthalmol 136(2):370–371. https://doi.org/10.1016/S0002-9394(03)00191-0
Simon S, de Thoisy B, Mercier A, Nacher M, Demar M (2019) Virulence of atypical Toxoplasma gondii strains isolated in French Guiana in a murine model. Parasite 26:60. https://doi.org/10.1051/parasite/2019048
Splendore A (1908) Un Nuovo Protozoa Parassita Deconigli Incontrato Nelle Lesioni Anatomiche d’une Malattia Che Ricorda in Molti Punti Il Kala-Azar Dell’uoma. Nota Preliminare Pel. Rev Soc Sci Sao Paulo 3.
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(7):841–848. https://doi.org/10.1016/j.ijpara.2006.03.003
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30:1217–1258. https://doi.org/10.1016/s0020-7519(00)00124-7.Erratum.In:IntJParasitol2001Feb;31(2):217-20
Valdès V, Legagneur H, Watrin V, Paris L, Hascoët JM (2011) Toxoplasmose congénitale secondaire à une réinfection maternelle pendant la grossesse [Congenital toxoplasmosis due to maternal reinfection during pregnancy]. Arch Pediatr 18(7):761–763. https://doi.org/10.1016/j.arcped.2011.04.011
Vasconcelos-Santos DV, Machado Azevedo DO, Campos WR, Oréfice F, Queiroz-Andrade GM, Carellos EV, Castro Romanelli RM, Januário JN, Resende LM, Martins-Filho OA, de Aguiar Vasconcelos Carneiro AC, Almeida Vitor RW, Caiaffa WT; UFMG Congenital Toxoplasmosis Brazilian Group (2009) Congenital toxoplasmosis in southeastern Brazil: results of early ophthalmologic examination of a large cohort of neonates. Ophthalmology. 116(11):2199-205.e1. https://doi.org/10.1016/j.ophtha.2009.04.042.
Vidal JE, Hernandez AV, de Oliveira AC, Dauar RF, Barbosa SP Jr, Focaccia R (2005) Cerebral toxoplasmosis in HIV-positive patients in Brazil: clinical features and predictors of treatment response in the HAART era. AIDS Patient Care STDS 19(10):626–634. https://doi.org/10.1089/apc.2005.19.626
Vidal JE, Oliveira AC (2013) AIDS-related cerebral toxoplasmosis in São Paulo State, Brazil: marked improvements in the highly active antiretroviral therapy-era but the challenges continue. Braz J Infect Dis 17(3):379–380. https://doi.org/10.1016/j.bjid.2012.10.030
Villena I, Aubert D, Leroux B, Dupouy D, Talmud M, Chemla C, Trenque T, Schmit G, Quereux C, Guenounou M, Pluot M, Bonhomme A, Pinon JM (1998) Pyrimethamine-sulfadoxine treatment of congenital toxoplasmosis: follow-up of 78 cases between 1980 and 1997. Reims Toxoplasmosis Group. Scand J Infect Dis 30(3):295–300. https://doi.org/10.1080/00365549850160963.
Webster JP, Lamberton PHL, McConkey GA (2016) The Toxoplasma gondii Model of Schizophrenia. In Handbook of Behavioral Neuroscience. Vol. 23. https://doi.org/10.1016/B978-0-12-800981-9.00014-6.
Wilson CB, Remington JS, Stagno S, Reynolds DW (1980) Development of adverse sequelae in children born with subclinical congenital Toxoplasma infection. Pediatrics 66(5):767–774
Witter R, Pena HFJ, Maia MO, de Magalhães AO, Morgado TO, Colodel EM, Barros DA, Igarashi M, Gennari SM, Pacheco RC (2020) Isolation and genotyping of Toxoplasma gondii in the Midwestern Brazil revealed high genetic diversity and new genotypes. Acta Trop 212:105681. https://doi.org/10.1016/j.actatropica.2020.105681
Xavier GA, Cademartori BG, Cunha Filho NA, Farias NA (2013) Evaluation of seroepidemiological toxoplasmosis in HIV/AIDS patients in the south of Brazil. Rev Inst Med Trop Sao Paulo 55(1):25–30. https://doi.org/10.1590/s0036-46652013000100005
Xiao J, Yolken RH (2015) Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol (oxf) 213(4):828–845. https://doi.org/10.1111/apha.12458
Xiao J, Buka SL, Cannon TD, Suzuki Y, Viscidi RP, Torrey EF, Yolken RH (2009) Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes Infect 11(13):1011–1018. https://doi.org/10.1016/j.micinf.2009.07.007
Funding
GLB, RWAV and ESMD are supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). RWAV (Process # 304815/2017–9) received the CNPq Research Productivity Scholarship.
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de Lima Bessa, G., de Almeida Vitor, R.W. & dos Santos Martins-Duarte, E. Toxoplasma gondii in South America: a differentiated pattern of spread, population structure and clinical manifestations. Parasitol Res 120, 3065–3076 (2021). https://doi.org/10.1007/s00436-021-07282-w
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DOI: https://doi.org/10.1007/s00436-021-07282-w