Ocular toxoplasmosis with positive polymerase chain reaction in peripheral blood – report of two cases, São Paulo State, Brazil

Authors

DOI:

https://doi.org/10.15448/1980-6108.2015.4.20932

Keywords:

Toxoplasma gondii, toxoplasmosis, ocular, retinochoroiditis, chorioretinitis, retinography, optical coherence tomography, PCR, polymerase chain reaction

Abstract

Aims: To describe the use of polymerase chain reaction (PCR) in peripheral blood and demonstrate its importance in the clinical follow-up of patients with ocular toxoplasmosis.

Case description: Two immunocompetent patients were clinically diagnosed with acute ocular toxoplasmosis. The routine clinical evaluation consisted of fundus examination using binocular indirect ophthalmoscopy, color fundus photography, fluorescein angiography, and spectral domain optical coherence tomography. The serological diagnosis was made by ELISA (IgM, IgG) and confirmed by ELFA (IgG, IgM). The molecular diagnosis was made by PCR in peripheral blood using the B1 gene of Toxoplasma gondii as marker. The younger patient was male, had previous lesion in the right eye, complained of low visual acuity in the left eye and was under treatment. The older patient was male, had retinal detachment, and presented with sudden loss of acuity in the right eye. The fundus examination revealed chorioretinal scar in the left eye. IgG was reactive, IgM was non-reactive, and PCR was positive in the peripheral blood of both patients. New blood samples were collected for serological and molecular monitoring and PCR remained positive in both cases. Six weeks after treatment with oral sulfadiazine and pyrimethamine, the PCR yielded negative results.

Conclusions: The results show that T. gondii antigens may be found in peripheral blood during ocular reactivations and that PCR may be a good tool for the follow-up of patients with ocular toxoplasmosis.

Downloads

Download data is not yet available.

References

Lopes AP, Dubey JP, Dardé M-L, Cardoso L. Epidemiological review of Toxoplasma gondii infection in humans and animals in Portugal. Parasitology. 2014;141(13):1699–708. http://dx.doi.org/10.1017/S0031182014001413

Malik A, Rizvi M, Khan F, Khan N, Rabbani T, Khan HM. Toxoplasma gondii in women with bad obstetric history and infertility: a five-year study. Asian Pac J Trop Dis. 2014;4:S236–9. http://dx.doi.org/10.1016/S2222-1808(14)60446-1

Nascimento LV, Stollar F, Tavares LB, Cavasini CE, Maia IL, Cordeiro JA, Ferreira MU. Risk factors for toxoplasmic encephalitis in HIV-infected patients: a case-control study in Brazil. Ann Trop Med Parasitol. 2001;95(6):587–93. http://dx.doi.org/10.1080/00034980120073931

Silva MMG. Neurologic complications of HIV in the HAART era: where are we? The Braz J Infect Dis. 2012;16(4):373–8. http://dx.doi.org/10.1016/j.bjid.2012.06.021

Dubey JP, Lago EG, Gennari SM, Su C, Jones JL. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology. 2012;139(11):1375–424. http://dx.doi.org/10.1017/S0031182012000765

Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, Belfort Jr R, Vítor RWA, Silveira C, Sibley LD. Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg Infect Dis. 2006;12(6):942–9. http://dx.doi.org/10.3201/eid1206.060025

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). Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Negl Trop Dis. 2008;2(8):e277. http://dx.doi.org/10.1371/journal.pntd.0000277

Pfaff AWA, De-la-Torre A, Rochet E, Brunet J, Sabou M, Sauer A, Bourcier T, Gomez-Marin JE, Candolfi E. New clinical and experimental insights into Old World and neotropical ocular toxoplasmosis. Int J Parasitol. 2014;44(2):99–107. http://dx.doi.org/10.1016/j.ijpara.2013.09.007

Maenz M, Schlüter D, Liesenfeld O, Schares G, Gross U, Pleyer U. Ocular toxoplasmosis past, present and new aspects of an old disease. Prog Retin Eye Res. 2014;39:77–106. http://dx.doi.org/10.1016/j.preteyeres.2013.12.005

Jones JL, Parise ME, Fiore AE. Neglected parasitic infections in the United States: toxoplasmosis. Am J Trop Med Hyg. 2014;90(5):794–9. http://dx.doi.org/10.4269/ajtmh.13-0722

Boothroyd JC, Grigg ME. Population biology of Toxoplasma gondii and its relevance to human infection: do different strains cause different disease? Curr Opin Microbiol. 2002;5(4):438–42. http://dx.doi.org/10.1016/S1369-5274(02)00349-1

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):767–73.e2. http://dx.doi.org/10.1016/j.ajo.2014.01.004

Furtado JMJ, Winthrop KLK, Butler NJ, Smith JR. Ocular toxoplasmosis I: parasitology, epidemiology and public health. Clin Experiment Ophthalmol. 2013;41(February):82–94. http://dx.doi.org/10.1111/j.1442-9071.2012.02821.x

Arantes TE, Silveira C, Holland GN, Muccioli C, Yu F, Jones JL, Goldhardt R, Lewis KG, Belfort R Jr. Ocular Involvement Following Post-natally Acquired Toxoplasma gondii Infection in Southern Brazil: A 28-Year Experience. Am J Ophthalmol. 2015. http://dx.doi.org/10.1016/j.ajo.2015.02.015

Ferreira AIC, De Mattos CCB, Frederico FB,Meira CS, Almeida GC Jr, Nakashima F, Bernardo CR, Pereira-Chioccola VL, De Mattos LC. Risk factors for ocular toxoplasmosis in Brazil. Epidemiol Infec. 2014;142(1):142–8. http://dx.doi.org/10.1017/S0950268813000526.

Rodrigues A, Uezato S, Vono M, Pandossio T; Spegiorin LCJF; Oliani AH; Vaz Oliani DCM; Brandão de Mattos CC; de Mattos LC. Non-association between anti-Toxoplasma gondii antibodies and ABO blood group system. J Venom Anim Toxins incl Trop Dis. 2011;17(2):184–9. http://dx.doi.org/10.1590/S1678-91992011000200009

Gonçalves MAS, Mattos CCB, Spegiorin LCJF, Oliani DCMV, Oliani AH, de Mattos LC. Seropositivity rates for toxoplasmosis, rubella, syphilis, cytomegalovirus, hepatitis and HIV among pregnant women receiving care at a public health service, São Paulo state, Brazil. Braz J Infect Dis. 2010;14(6):601–5. http://dx.doi.org/10.1016/S1413-8670(10)70118-5

Mattos CCB, Cintra JR, Ferreira AIC, Spegiorin LCJF, Galisteu KJ, Machado RLD, de Mattos LC. Lack of association between ABO histo-blood groups, secretor and non-secretor phenotypes, and anti-Toxoplasma gondii antibodies among pregnant women from the northwestern region of Sao Paulo State, Brazil. Arch Med Sci. 2008;4(3):254–8.

Mendes NHD, Oliveira CBS, Garcia CA, Holanda CMXC, Andrade-Neto VF. Epidemiological and serological profiles of ocular toxoplasmosis in the municipality of Natal, northeastern Brazil. Trans R Soc Trop Med Hyg. 2014;108(10):656–61. http://dx.doi.org/10.1093/trstmh/tru113

Dantas SSBA, Fernandes ARF, Souza Neto OL, Mota RA, Alves CJ, Azevedo SS. Occurrence and risk factors associated with Toxoplasma gondii and Neospora caninum infections in dogs in the county of Natal, Rio Grande do Norte state, Northeastern Brazil. Ciência Rural. 2013;43(11):2042–8. http://dx.doi.org/10.1590/S0103-84782013001100020

Silva LLA, Andrade RRO, Carneiro ACA V, Vitor RRWA. Overlapping Toxoplasma gondii Genotypes Circulating in Domestic Animals and Humans in Southeastern Brazil. PloS One. 2014;9(2):e90237. http://dx.doi.org/10.1371/journal.pone.0090237

Costa JG, Carneiro AC, Tavares AT, Andrade GM, Vasconcelos-Santos DV, Januário JN, Menezes-Souza D, Fujiwara RT, Vitor RW. Real-time PCR as a prognostic tool for human congenital toxoplasmosis. J Clin Microbiol. 2013;51(8):2766–8. http://dx.doi.org/10.1128/JCM.00982-13

Previato M, Frederico FB, Murata FH, Siqueira RC, Barbosa AP, Silveira-Carvalho AP, Meira CS, Pereira-Chioccola VL, Gava R, Martins Neto PP, de Mattos LC, Brandão de Mattos CC. A Brazilian report using serological and molecular diagnosis to monitoring acute ocular toxoplasmosis. BMC Res Notes. 2015; 8:746. http://dx.doi.org/10.1186/s13104-015-1650-6

Fricker-Hidalgo H, Cimon B, Chemla C, Darde ML, Delhaes L, L'ollivier C, Godineau N, Houze S, Paris L, Quinio D, Robert-Gangneux F, Villard O, Villena I, Candolfi E, Pelloux H. Toxoplasma seroconversion with negative or transient immunoglobulin M in pregnant women: myth or reality? A French multicentre retrospective study. J Clin Microbiol. 2013;51(7):2103–11. http://dx.doi.org/10.1128/JCM.00169-13

Mattos CCB, Meira CS, Ferreira AIC, Frederico FB, Hiramoto RM, Jr GC, Mattos LC, Pereira-Chioccola VL. Contribution of laboratory methods in diagnosing clinically suspected ocular toxoplasmosis in Brazilian patients. Diagn Microbiol Infect Dis. 2011;70(3):362–6. http://dx.doi.org/10.1016/j.diagmicrobio.2011.02.002

Novais EA, Commodaro AG, Santos F, Muccioli C, Maia A, Nascimento H, Moeller CT, Rizzo LV, Grigg ME, Belfort R Jr. Patients with diffuse uveitis and inactive toxoplasmic retinitis lesions test PCR positive for Toxoplasma gondii in their vitreous and blood. Br J Ophthalmol. 2014;98(7):937–40. http://dx.doi.org/10.1136/bjophthalmol-2013-304184

Oréfice JL, Costa RA, Scott IU, Calucci D, Oréfice F. Spectral optical coherence tomography findings in patients with ocular toxoplasmosis and active satellite lesions (MINAS Report 1). Acta Ophthalmol. 2013;91(1):e41–7. http://dx.doi.org/10.1111/j.1755-3768.2012.02531.x

Villard O, Cimon B, L'Ollivier C, Fricker-Hidalgo H, Godineau N, Houze S, Paris L, Pelloux H, Villena I, Candolfi E. Serological Diagnosis of Toxoplasma gondii Infection: Recommendations from the French National Reference Center for Toxoplasmosis. Diagn Microbiol Infect Dis. 2015;84(1):22–33. http://dx.doi.org/10.1016/j.diagmicrobio.2015.09.009

Blanco PJ, Assia YM, Montero YM, Orozco KE. ELFA IgG anti-Toxoplasma y PCR anidada para el diagnóstico de toxoplasmosis en mujeres gestantes de Sincelejo, Colombia. Infectio. 2011;15(4):253–8. http://dx.doi.org/10.1016/S0123-9392(11)70739-1

Silveira C, Vallochi AL, Rodrigues da Silva U, Muccioli C, Holland GN, Nussenblatt RB, Belfort R, Rizzo LV. Toxoplasma gondii in the peripheral blood of patients with acute and chronic toxoplasmosis. Br J Ophthalmol. 2011;95(3):396–400. http://dx.doi.org/10.1136/bjo.2008.148205

Gómez-Marín JEJ, de-la-Torre A, Barrios P, Cardona N, Álvarez C, Herrera C. Toxoplasmosis in military personnel involved in jungle operations. Acta Trop. 2012;122(1):46–51. http://dx.doi.org/10.1016/j.actatropica.2011.11.019

Andújar BR, Pe-a MSR, Nodarse JF, Rivero LR, Fernandéz FAN, Puebla LEJ. Aplicación de herramientas serológicas y moleculares para el diagnóstico de coriorretinitis por Toxoplasma gondii. Rev Cubana Med Trop. 2013;65(1):13–25.

Sull AC, Vuong LN, Price LL, Srinivasan VJ, Gorczynska I, Fujimoto JG, Schuman JS, Duker JS. Comparison of spectral/Fourier domain optical coherence tomography instruments for assessment of normal macular thickness. Retina. 2010;30(2):235–45. http://dx.doi.org/10.1097/IAE.0b013e3181bd2c3b

Belaz S, Gangneux J-P, Dupretz P, Guiguen C, Robert-Gangneux F. A 10-year retrospective comparison of two target sequences, REP-529 and B1, for Toxoplasma gondii detection by quantitative PCR. J Clin Microbiol. 2015;53(4):JCM.02900–14. http://dx.doi.org/10.1128/JCM.02900-14

Olariu TR, Remington JS, Montoya JG. Polymerase chain reaction in cerebrospinal fluid for the diagnosis of congenital toxoplasmosis. Pediatr Infect Dis J. 2014;33(6):566–70. http://dx.doi.org/10.1097/INF.0000000000000256

Barbosa MA, Angelin LG, Saikawa GIA, Oliveira CJS, Silva SS, Vendruscolo JW, Marinello PC, Fujita TC, Rocha SPD, Watanabe MAE, Mitsuka-Bregano R, Costa IN. Potenciais alternativas terapêuticas em estudo para a toxoplasmose congênita: uma revisão bibliográfica. Rev Patol Trop. 2015:44:1–11. http://dx.doi.org/10.5216/rpt.v44i1.34798

Mancini DT, Assis LC, Ramalho TC, Cunha EF, Franca TCC. Toxoplasmose: Perspectivas no Estudo de Novos Alvos Terapêuticos. Rev Virt Quím. 2012;4(4):434–55.

Paquet C, Yudin MH. Toxoplasmosis in pregnancy: prevention, screening, and treatment. J Obstet Gynaecol Can. 2013;35(1):78–81. http://dx.doi.org/10.1016/S1701-2163(15)31053-7

Nakao M, Yamamoto I, Yamamoto H. Successful treatment of ocular toxoplasmosis that developed four years after kidney transplantation. Transpl Int.2015;28(3):363-5. http://dx.doi.org/10.1111/tri.12433

Schallhorn JM, Gonzales J. Ocular toxoplasmosis: the treatment dilemma. J AAPOS. 2013;17(5):454–5. http://dx.doi.org/10.1016/j.jaapos.2013.08.001

Kijlstra A, Petersen E. Epidemiology, pathophysiology, and the future of ocular toxoplasmosis. Ocul Immunol Inflamm. 2014;22(2):138–47. http://dx.doi.org/10.3109/09273948.2013.823214

Pleyer U, Alió JL, Barisani-Asenbauer T, Le Hoang P, Rao NA. Immune Modulation and Anti-Inflammatory Therapy in Ocular Disorders. Berlin, Heidelberg: Springer Berlin Heidelberg; 2014. http://dx.doi.org/10.1007/978-3-642-54350-0

Jensen KD, Camejo A, Melo MB, Cordeiro C, Julien L, Grotenbreg GM, Frickel EM, Ploegh HL, Young L, Saeij JP. Toxoplasma gondii Superinfection and Virulence during Secondary Infection Correlate with the Exact ROP5/ROP18 Allelic Combination. mBio. 2015;6(2):e02280-14. http://dx.doi.org/10.1128/mBio.02280-14

Avelino MM, Amaral WN, Rodrigues IM, Rassi AR, Gomes MB, Costa TL, Castro AM. Congenital toxoplasmosis and prenatal care state programs. BMC Infect Dis. 2014;14(1):33. http://dx.doi.org/10.1186/1471-2334-14-33

Grigg ME, Dubey JP, Nussenblatt RB. Ocular toxoplasmosis: lessons from Brazil. Am J Ophthalmol. 2015;159(6):999–1001. http://dx.doi.org/10.1016/j.ajo.2015.04.005

Published

2016-02-25

How to Cite

Barbosa, A. P., Frederico, F. B., Previato, M., Ferreira, A. I. da C., Martins Neto, P. P., Meira, C. da S., … Brandão de Mattos, C. C. (2016). Ocular toxoplasmosis with positive polymerase chain reaction in peripheral blood – report of two cases, São Paulo State, Brazil. Scientia Medica, 25(4), ID20932. https://doi.org/10.15448/1980-6108.2015.4.20932

Issue

Section

Case Reports

Most read articles by the same author(s)