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Invited Review

Pathophysiological Aspects of Ocular Toxoplasmosis: Host-parasite Interactions

, MD, MSc, PhDcORCID Icon, , MD, PhD, , MD, PhD, , MBChB, FRCOphth, MMedEd, , PhD, , MD, PhDc, , FRCOphth, , MD, PhD & , MD, PhDORCID Icon show all
Pages 560-569 | Received 06 Nov 2020, Accepted 19 Apr 2021, Published online: 09 Jul 2021

References

  • Saadatnia G, Golkar M. A review on human toxoplasmosis. Scand J Infect Dis. 2012;44(11):805–814. doi:10.3109/00365548.2012.693197.
  • Soheilian M, Heidari K, Yazdani S, Shahsavari M, Ahmadieh H, Dehghan M. Patterns of uveitis in a tertiary eye care center in Iran. Ocul Immunol Inflamm. 2004;12(4):297–310. doi:10.1080/092739490500174.
  • Wakefield D, Dunlop I, McCluskey PJ, Penny R. Uveitis: aetiology and disease associations in an Australian population. Aust N Z J Ophthalmol. 1986;14(3):181–187. doi:10.1111/j.1442-9071.1986.tb00034.x.
  • Xiao J, Yolken RH. Strain hypothesis of Toxoplasma gondii infection on the outcome of human diseases. Acta Physiol (Oxf). 2015;213(4):828–845. doi:10.1111/apha.12458.
  • Sánchez V, De-la-torre A, Gómez-Marín JE. Characterization of ROP18 alleles in human toxoplasmosis. Parasitol Int. 2014;63(2):463–469. doi:10.1016/j.parint.2013.10.012.
  • Arantes TEF, Silveira C, Holland GN, et al. Ocular involvement following postnatally acquired Toxoplasma gondii infection in Southern Brazil: a 28-year experience. Am J Ophthalmol. 2015;159(6):1002–1012.e2. doi:10.1016/j.ajo.2015.02.015.
  • Naranjo-Galvis CA, De-la-torre A, Mantilla-Muriel LE, et al. Genetic polymorphisms in cytokine genes in colombian patients with ocular toxoplasmosis. Infect Immun. 2018;86(4):e00597–17. doi:10.1128/IAI.00597-17.
  • De Albuquerque MC, Do Aleixo Alq C, Benchimol EI, et al. The IFN-gamma +874T/A gene polymorphism is associated with retinochoroiditis toxoplasmosis susceptibility. Memorias Inst Oswaldo Cruz. 2009;104(3):451–455. doi:10.1590/s0074-02762009000300009.
  • Cordeiro CA, Moreira PR, Andrade MS, et al. Interleukin-10 gene polymorphism (−1082G/A) is associated with toxoplasmic retinochoroiditis. Invest Ophthalmol Vis Sci. 2008;49(5):1979–1982. doi:10.1167/iovs.07-1393.
  • Cordeiro CA, Moreira PR, Costa GC, et al. TNF-alpha gene polymorphism (−308G/A) and toxoplasmic retinochoroiditis. Br J Ophthalmol. 2008;92(7):986–988. doi:10.1136/bjo.2008.140590.
  • Cordeiro CA, Moreira PR, Bessa TF, et al. Interleukin-6 gene polymorphism (−174 G/C) is associated with toxoplasmic retinochoroiditis. Acta Ophthalmol. 2013;91(4):e311–314. doi:10.1111/aos.12046.
  • Pfaff AW, De-la-torre A, Rochet E, et al. New clinical and experimental insights into old world and neotropical ocular toxoplasmosis. Int J Parasitol. 2014;44(2):99–107. doi:10.1016/j.ijpara.2013.09.007.
  • Garweg JG, Candolfi E. Immunopathology in ocular toxoplasmosis: facts and clues. Mem Inst Oswaldo Cruz. 2009;104(2):211–220. doi:10.1590/s0074-02762009000200014.
  • Bahia-Oliveira LM, Dardé M-L, Amendoeira MRR. Toxoplasma gondii centennial anniversary: 100 years of research to celebrate all over the world. Memórias Inst Oswaldo Cruz. 2009;104(2):129–131. doi:10.1590/S0074-02762009000200002.
  • Hogan MJ. Ocular toxoplasmosis. Am J Ophthalmol. 1958;46(4):467–494. doi:10.1016/0002-9394(58)91127-9.
  • Mukhopadhyay D, Arranz-Solís D, Saeij JPJ. Influence of the host and parasite strain on the immune response during Toxoplasma infection. Front Cell Infect Microbiol. 2020;10. doi:10.3389/fcimb.2020.580425.
  • Yan C, Liang L-J, Zheng K-Y, Zhu X-Q. Impact of environmental factors on the emergence, transmission and distribution of Toxoplasma gondii. Parasit Vectors. 2016;9. doi:10.1186/s13071-016-1432-6.
  • Shwab EK, Saraf P, Zhu X-Q, et al. Human impact on the diversity and virulence of the ubiquitous zoonotic parasite Toxoplasma gondii. PNAS. 2018;115(29):E6956–E6963. doi:10.1073/pnas.1722202115.
  • Cordeiro CA, Moreira PR, Costa GC, et al. Interleukin-1 gene polymorphisms and toxoplasmic retinochoroiditis. Mol Vis. 2008;14:1845–1849.
  • Jamieson SE, De Roubaix L-A, Cortina-Borja M, et al. Genetic and epigenetic factors at COL2A1 and ABCA4 influence clinical outcome in congenital toxoplasmosis. PLoS ONE. 2008;3(6):e2285. doi:10.1371/journal.pone.0002285.
  • Peixoto-Rangel AL, Miller EN, Castellucci L, et al. Candidate gene analysis of ocular toxoplasmosis in Brazil: evidence for a role for toll-like receptor 9 (TLR9). Mem Inst Oswaldo Cruz. 2009;104(8):1187–1190. doi:10.1590/s0074-02762009000800019.
  • Jamieson SE, Peixoto-Rangel AL, Hargrave AC, et al. Evidence for associations between the purinergic receptor P2X(7) (P2RX7) and toxoplasmosis. Genes Immun. 2010;11(5):374–383. doi:10.1038/gene.2010.31.
  • Lees MP, Fuller SJ, McLeod R, et al. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. J Immunol. 2010;184(12):7040–7046. doi:10.4049/jimmunol.1000012.
  • Tan TG, Mui E, Cong H, et al. Identification of T. gondii epitopes, adjuvants, and host genetic factors that influence protection of mice and humans. Vaccine. 2010;28(23):3977–3989. doi:10.1016/j.vaccine.2010.03.028.
  • Witola WH, Mui E, Hargrave A, et al. NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells. Infect Immun. 2011;79(2):756–766. doi:10.1128/IAI.00898-10.
  • Dutra MS, Béla SR, Peixoto-Rangel AL, et al. Association of a NOD2 gene polymorphism and T-helper 17 cells with presumed ocular toxoplasmosis. J Infect Dis. 2013;207(1):152–163. doi:10.1093/infdis/jis640.
  • Peixe RG, Boechat MSB, Rangel ALP, Rosa RFG, Petzl-Erler ML, Bahia-Oliveira LMG. Single nucleotide polymorphisms in the interferon gamma gene are associated with distinct types of retinochoroidal scar lesions presumably caused by Toxoplasma gondii infection. Mem Inst Oswaldo Cruz. 2014;109(1):99–107. doi:10.1590/0074-0276140539.
  • Witola WH, Liu SR, Montpetit A, et al. ALOX12 in human toxoplasmosis. Infect Immun. 2014;82(7):2670–2679. doi:10.1128/IAI.01505-13.
  • Wujcicka W, Gaj Z, Wilczyński J, Nowakowska D. Contribution of IL6-174 G>C and IL1B +3954 C>T polymorphisms to congenital infection with Toxoplasma gondii. Eur J Clin Microbiol Infect Dis. 2015;34(11):2287–2294. doi:10.1007/s10096-015-2481-z.
  • Wujcicka W, Wilczyński J, Nowakowska D. Genetic alterations within TLR genes in development of Toxoplasma gondii infection among Polish pregnant women. Adv Med Sci. 2017;62(2):216–222. doi:10.1016/j.advms.2017.02.002.
  • Minns LA, Menard LC, Foureau DM, et al. TLR9 is required for the gut-associated lymphoid tissue response following oral infection of Toxoplasma gondii. J Immunol. 2006;176(12):7589–7597. doi:10.4049/jimmunol.176.12.7589.
  • Gorfu G, Cirelli KM, Melo MB, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. mBio. 2014;5(1). doi:10.1128/mBio.01117-13.
  • Huang S-W, Walker C, Pennock J, et al. P2X7 receptor-dependent tuning of gut epithelial responses to infection. Immunol Cell Biol. 2017;95(2):178–188. doi:10.1038/icb.2016.75.
  • Cong H, Mui EJ, Witola WH, et al. Human immunome, bioinformatic analyses using HLA supermotifs and the parasite genome, binding assays, studies of human T cell responses, and immunization of HLA-A*1101 transgenic mice including novel adjuvants provide a foundation for HLA-A03 restricted CD8+T cell epitope based, adjuvanted vaccine protective against Toxoplasma gondii. Immunome Res. 2010;6:12. doi:10.1186/1745-7580-6-12.
  • Remington and Klein’s Infectious Diseases of the Fetus and Newborn Infant. 8th ed. https://www.elsevier.com/books/remington-and-kleins-infectious-diseases-of-the-fetus-and-newborn-infant/wilson/978-0-323-24147-2. Accessed July 15, 2020.
  • Holland GN. Ocular toxoplasmosis in the immunocompromised host. Int Ophthalmol. 1989;13(6):399–402. doi:10.1007/BF02306488.
  • Cochereau-Massin I, LeHoang P, Lautier-Frau M, et al. Ocular toxoplasmosis in human immunodeficiency virus-infected patients. Am J Ophthalmol. 1992;114(2):130–135. doi:10.1016/s0002-9394(14)73975-3.
  • Moshfeghi DM, Dodds EM, Couto CA, et al. Diagnostic approaches to severe, atypical toxoplasmosis mimicking acute retinal necrosis. Ophthalmology. 2004;111(4):716–725. doi:10.1016/j.ophtha.2003.07.004.
  • De-la-torre A, Gómez-Marín J. Disease of the year 2019: ocular toxoplasmosis in HIV-infected patients. Ocul Immunol Inflamm. 2020;28(7):1031–1039. doi:10.1080/09273948.2020.1735450.
  • Yeo JH, Jakobiec FA, Iwamoto T, Richard G, Kreissig I. Opportunistic toxoplasmic retinochoroiditis following chemotherapy for systemic lymphoma. A light and electron microscopic study. Ophthalmology. 1983;90(8):885–898. doi:10.1016/s0161-6420(83)80012-8.
  • Johnson MW, Greven GM, Jaffe GJ, Sudhalkar H, Vine AK. Atypical, severe toxoplasmic retinochoroiditis in elderly patients. Ophthalmology. 1997;104(1):48–57. doi:10.1016/s0161-6420(97)30362-5.
  • Grubeck-Loebenstein B, Wick G. The aging of the immune system. Adv Immunol. 2002;80:243–284. doi:10.1016/s0065-2776(02)80017-7.
  • Suzuki Y, Joh K, Orellana MA, Conley FK, Remington JS. A gene(s) within the H-2D region determines the development of toxoplasmic encephalitis in mice. Immunology. 1991;74:732–739.
  • Suzuki Y, Wong SY, Grumet FC, et al. Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J Infect Dis. 1996;173(1):265–268. doi:10.1093/infdis/173.1.265.
  • Mack DG, Johnson JJ, Roberts F, et al. HLA-class II genes modify outcome of Toxoplasma gondii infection. Int J Parasitol. 1999;29(9):1351–1358. doi:10.1016/s0020-7519(99)00152-6.
  • Meenken C, Rothova A, De Waal LP, Van der Horst AR, Mesman BJ, Kijlstra A. HLA typing in congenital toxoplasmosis. British J Ophthalmol. 1995;79(5):494–497. doi:10.1136/bjo.79.5.494.
  • Holland GN, Cornell PJ, Park MS, et al. An association between acute retinal necrosis syndrome and HLA-DQw7 and phenotype Bw62, DR4. Am J Ophthalmol. 1989;108(4):370–374. doi:10.1016/s0002-9394(14)73303-3.
  • Nussenblatt RB, Mittal KK, Fuhrman S, Sharma SD, Palestine AG. Lymphocyte proliferative responses of patients with ocular toxoplasmosis to parasite and retinal antigens. Am J Ophthalmol. 1989;107(6):632–641. doi:10.1016/0002-9394(89)90260-2.
  • Yamamoto JH, Vallochi AL, Silveira C, et al. Discrimination between patients with acquired toxoplasmosis and congenital toxoplasmosis on the basis of the immune response to parasite antigens. J Infect Dis. 2000;181(6):2018–2022. doi:10.1086/315494.
  • Cone RE, Pais R. Anterior Chamber-Associated Immune Deviation (ACAID): an acute response to ocular insult protects from future immune-mediated damage? Ophthalmol Eye Dis. 2009;1:33–40. doi:10.4137/OED.S2858.
  • Niederkorn JY. Immune privilege in the anterior chamber of the eye. Crit Rev Immunol. 2002;22(1):13–46. doi:10.1615/CritRevImmunol.v22.i1.20.
  • Niederkorn JY. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat Immunol. 2006;7(4):354–359. doi:10.1038/ni1328.
  • Stein-Streilein J, Streilein JW. Anterior chamber associated immune deviation (ACAID): regulation, biological relevance, and implications for therapy. Int Rev Immunol. 2002;21(2–3):123–152. doi:10.1080/08830180212066.
  • Cone R, Chattopadhyay S, O’Rourke J. Control of delayed-type hypersensitivity by ocular- induced CD8+ regulatory t cells. Chem Immunol Allergy. 2008;94:138–149. doi:10.1159/000154998.
  • Wilbanks GA, Mammolenti M, Streilein JW. Studies on the induction of anterior chamber-associated immune deviation (ACAID). II. Eye-derived cells participate in generating blood-borne signals that induce ACAID. J Immunol. 1991;146:3018–3024.
  • Wang Y, Goldschneider I, O’Rourke J, Cone RE. Blood mononuclear cells induce regulatory NK T thymocytes in anterior chamber-associated immune deviation. J Leukoc Biol. 2001;69:741–746.
  • Li X, Wang Y, Urso D, O’Rourke J, Cone RE. Thymocytes induced by antigen injection into the anterior chamber activate splenic CD8+ suppressor cells and enhance the antigen-induced production of immunoglobulin G1 antibodies. Immunology. 2004;113(1):44–56. doi:10.1111/j.1365-2567.2004.01928.x.
  • Li X, Shen S, Urso D, et al. Phenotypic and immunoregulatory characteristics of monocytic iris cells. Immunology. 2006;117(4):566–575. doi:10.1111/j.1365-2567.2006.02333.x.
  • Hara Y, Okamoto S, Rouse B, Streilein JW. Evidence that peritoneal exudate cells cultured with eye-derived fluids are the proximate antigen-presenting cells in immune deviation of the ocular type. J Immunol. 1993;151:5162–5171.
  • Greigert V, Bittich-Fahmi F, Pfaff AW. Pathophysiology of ocular toxoplasmosis: facts and open questions. PLoS Negl Trop Dis. 2020;14(12):e0008905. doi:10.1371/journal.pntd.0008905.
  • Holland GN. Ocular toxoplasmosis: a global reassessment. Part II: disease manifestations and management. Am J Ophthalmol. 2004;137:1–17.
  • Bosch-Driessen LEH, Berendschot TTJM, Ongkosuwito JV, Rothova A. Ocular toxoplasmosis: clinical features and prognosis of 154 patients. Ophthalmology. 2002;109(5):869–878. doi:10.1016/s0161-6420(02)00990-9.
  • Holland GN. Ocular toxoplasmosis: the influence of patient age. Mem Inst Oswaldo Cruz. 2009;104(2):351–357. doi:10.1590/s0074-02762009000200031.
  • Holland GN, Crespi CM, Ten Dam-van Loon N, et al. Analysis of recurrence patterns associated with toxoplasmic retinochoroiditis. Am J Ophthalmol. 2008;145(6):1007–1013. doi:10.1016/j.ajo.2008.01.023.
  • Garweg JG, Scherrer J, Wallon M, Kodjikian L, Peyron F. Reactivation of ocular toxoplasmosis during pregnancy. BJOG. 2005;112(2):241–242. doi:10.1111/j.1471-0528.2004.00302.x.
  • Silveira C, Ferreira R, Muccioli C, Nussenblatt R, Belfort R. Toxoplasmosis transmitted to a newborn from the mother infected 20 years earlier. Am J Ophthalmol. 2003;136(2):370–371. doi:10.1016/s0002-9394(03)00191-0.
  • Andrade GMQ, Vasconcelos-Santos DV, Carellos EVM, et al. Congenital toxoplasmosis from a chronically infected woman with reactivation of retinochoroiditis during pregnancy. J Pediatr (Rio J). 2010;86(1):85–88. doi:10.2223/JPED.1948.
  • Kalogeropoulos D, Sung VC, Paschopoulos M, Moschos MM, Panidis P, Kalogeropoulos C. The physiologic and pathologic effects of pregnancy on the human visual system. J Obstet Gynaecol. 2019;39(8):1037–1048. doi:10.1080/01443615.2019.1584891.
  • Gómez-Chávez F, Cañedo-Solares I, Ortiz-Alegría LB, et al. Maternal immune response during pregnancy and vertical transmission in human toxoplasmosis. Front Immunol. 2019;10. doi:10.3389/fimmu.2019.00285.
  • Kodjikian L, Hoigne I, Adam O, et al. Vertical transmission of toxoplasmosis from a chronically infected immunocompetent woman. Pediatr Infect Dis J. 2004;23(3):272–274. doi:10.1097/01.inf.0000115949.12206.69.
  • Friedmann CT, Knox DL. Variations in recurrent active toxoplasmic retinochoroiditis. Arch Ophthalmol. 1969;81(4):481–493. doi:10.1001/archopht.1969.00990010483005.
  • O’Connor GR. Factors related to the initiation and recurrence of uveitis. XL Edward Jackson memorial lecture. Am J Ophthalmol. 1983;96(5):577–599. doi:10.1016/s0002-9394(14)73415-4.
  • Braakenburg AMD, Crespi CM, Holland GN, Wu S, Yu F, Rothova A. Recurrence rates of ocular toxoplasmosis during pregnancy. Am J Ophthalmol. 2014;157(4):767–773.e2. doi:10.1016/j.ajo.2014.01.004.
  • Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature. 1992;359(6390):82–85. doi:10.1038/359082a0.
  • Howe DK, Sibley LD. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. J Infect Dis. 1995;172(6):1561–1566. doi:10.1093/infdis/172.6.1561.
  • Su C, Khan A, Zhou P, et al. Globally diverse Toxoplasma gondii isolates comprise six major clades originating from a small number of distinct ancestral lineages. PNAS. 2012;109(15):5844–5849. doi:10.1073/pnas.1203190109.
  • Sibley LD, Ajioka JW. Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu Rev Microbiol. 2008;62:329–351. doi:10.1146/annurev.micro.62.081307.162925.
  • Bertranpetit E, Jombart T, Paradis E, et al. Phylogeography of Toxoplasma gondii points to a South American origin. Infect Genet Evol. 2017;48:150–155. doi:10.1016/j.meegid.2016.12.020.
  • Alvarez C, De-la-torre A, Vargas M, et al. Striking divergence in Toxoplasma ROP16 nucleotide sequences from human and meat samples. J Infect Dis. 2015;211(12):2006–2013. doi:10.1093/infdis/jiu833.
  • De-la-torre A, Sauer A, Pfaff AW, et al. 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. 2013;7(11):e2541. doi:10.1371/journal.pntd.0002541.
  • Niedelman W, Gold DA, Rosowski EE, et al. The rhoptry proteins ROP18 and ROP5 mediate Toxoplasma gondii evasion of the murine, but not the human, interferon-gamma response. PLoS Pathog. 2012;8(6):e1002784. doi:10.1371/journal.ppat.1002784.
  • Saeij JPJ, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC. Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect Immun. 2005;73(2):695–702. doi:10.1128/IAI.73.2.695-702.2005.
  • De-la-torre A, Pfaff AW, Grigg ME, Villard O, Candolfi E, Gomez-Marin JE. Ocular cytokinome is linked to clinical characteristics in ocular toxoplasmosis. Cytokine. 2014;68(1):23–31. doi:10.1016/j.cyto.2014.03.005.
  • Torres-Morales E, Taborda L, Cardona N, et al. Th1 and Th2 immune response to P30 and ROP18 peptides in human toxoplasmosis. Med Microbiol Immunol. 2014;203(5):315–322. doi:10.1007/s00430-014-0339-0.
  • Vasconcelos-Santos DV, Machado Azevedo DO, Campos WR, et al. Congenital Toxoplasmosis in Southeastern Brazil: results of early ophthalmologic examination of a large cohort of neonates. Ophthalmology. 2009;116(11):2199–2205.e1. doi:10.1016/j.ophtha.2009.04.042.
  • McLeod R, Boyer KM, Lee D, et al. Prematurity and severity are associated with Toxoplasma gondii alleles (NCCCTS, 1981-2009). Clinic Infect Diseases. 2012;54(11):1595–1605. doi:10.1093/cid/cis258.
  • Carme B, Bissuel F, Ajzenberg D, et al. Severe acquired toxoplasmosis in immunocompetent adult patients in French Guiana. J Clin Microbiol. 2002;40(11):4037–4044. doi:10.1128/jcm.40.11.4037-4044.2002.
  • Demar M, Ajzenberg D, Maubon D, et al. Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects. Clinic Infect Diseases. 2007;45(7):e88–95. doi:10.1086/521246.
  • Cortés DA, Aguilar MC, Ríos HA, et al. Severe acute multi-systemic failure with bilateral ocular toxoplasmosis in immunocompetent patients from urban settings in Colombia: case reports. Am J Ophthalmol Case Rep. 2020;18:100661. doi:10.1016/j.ajoc.2020.100661.
  • Feustel SM, Meer M, Liesenfeld O. Toxoplasma gondii and the blood-brain barrier. Virulence. 2012;3(2):182–192. doi:10.4161/viru.19004.
  • Lachenmaier SM, Deli MA, Meer M, Liesenfeld O. Intracellular transport of Toxoplasma gondii through the blood-brain barrier. J Neuroimmunol. 2011;232(1–2):119–130. doi:10.1016/j.jneuroim.2010.10.029.
  • Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gâtel D, Tardieux I. CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood. 2006;107(1):309–316. doi:10.1182/blood-2005-02-0666.
  • Sauer A, Rochet E, Lahmar I, et al. The local immune response to intraocular Toxoplasma re-challenge: less pathology and better parasite control through Treg/Th1/Th2 induction. Int J Parasitol. 2013;43(9):721–728. doi:10.1016/j.ijpara.2013.04.004.
  • Guiton R, Vasseur V, Charron S, et al. Interleukin 17 receptor signaling is deleterious during Toxoplasma gondii infection in susceptible BL6 mice. J Infect Dis. 2010;202(3):427–435. doi:10.1086/653738.
  • O’Connor W, Kamanaka M, Booth CJ, et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol. 2009;10(6):603–609. doi:10.1038/ni.1736.
  • Sauer A, Pfaff AW, Villard O, et al. Interleukin 17A as an effective target for anti-inflammatory and antiparasitic treatment of toxoplasmic uveitis. J Infect Dis. 2012;206(8):1319–1329. doi:10.1093/infdis/jis486.
  • Simsek M, Ozdal PC, Kocer AM. Optic nerve involvement in ocular toxoplasmosis: 12 year data from a tertiary referral center in Turkey. Arq Bras Oftalmol. 2019;82(4):302–309. doi:10.5935/0004-2749.20190058.
  • De Souza EC, Casella AMB. Clinical and tomographic features of macular punctate outer retinal toxoplasmosis. Arch Ophthalmol. 2009;127(10):1390–1394. doi:10.1001/archophthalmol.2009.251.
  • Dubey JP, Graham DH, Blackston CR, et al. Biological and genetic characterisation of Toxoplasma gondii isolates from chickens (Gallus domesticus) from São Paulo, Brazil: unexpected findings. Int J Parasitol. 2002;32(1):99–105. doi:10.1016/s0020-7519(01)00364-2.
  • Shapiro K, Bahia-Oliveira L, Dixon B, et al. Environmental transmission of Toxoplasma gondii: oocysts in water, soil and food. Food Waterborne Parasitol. 2019;15:e00049. doi:10.1016/j.fawpar.2019.e00049.
  • Gómez-Marin JE, De-la-torre A, Angel-Muller E, et al. First Colombian multicentric newborn screening for congenital toxoplasmosis. PLoS Negl Trop Dis. 2011;5(5):e1195. doi:10.1371/journal.pntd.0001195.
  • Rudzinski M, Meyer A, Khoury M, Couto C. Is reactivation of toxoplasmic retinochoroiditis associated to increased annual rainfall? Parasite. 2013;20:44. doi:10.1051/parasite/2013044.
  • Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB. Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol. 2001;154(4):357–365. doi:10.1093/aje/154.4.357.
  • Gilbert RE, Stanford MR, Jackson H, Holliman RE, Sanders MD. Incidence of acute symptomatic toxoplasma retinochoroiditis in south London according to country of birth. BMJ. 1995;310(6986):1037–1040. doi:10.1136/bmj.310.6986.1037.

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