PURPOSE: To report the findings of indocyanine green angiography performed in patients with recurrent ocular toxoplasmosis. METHODS: Institutional prospective analysis of 23 eyes from 23 immunocompetent patients with recurrent ocular toxoplasmosis aged between 17 and 41 years. These patients underwent a complete ocular examination including indocyanine green angiography. RESULTS: Multiple hypofluorescent spots distant from the recurrent active lesion of retinochoroidal toxoplasmosis were found in 26.08% of the patients. We also found multiple hypofluorescent satellite dots in 69.56% of the patients. CONCLUSION: These remote dots seen suggest either a more widespread choroidal involvement in this disease and this can represent simply remote collections of inflammatory cells or subclinical infection.OBJETIVOS: Relatar os achados da angiografia com indocianina verde, realizados em pacientes com recidiva de toxoplasmose ocular. MÉTODOS: Análise institucional e prospectiva de 23 olhos de 23 pacientes, imunocompetentes com idades entre 17 e 41 anos. Estes pacientes foram submetidos a exame oftalmológico de rotina e a angiografia com indocianina verde. RESULTADOS: Foram encontrados múltiplos pontos hipofluorescentes distantes da lesão ativa recidivada da toxoplasmose retino-coroidiana em 26,08% dos casos, chamados por nós de pontos remotos e encontramos também, pontos hipofluorescentes circundando ou próximos da lesão ativa recidivada em 69,56% dos casos. CONCLUSÃO: Os pontos hipofluorescentes distantes da lesão ativa recidivada, chamados de pontos remotos, não descritos previamente na doença, demonstram um maior envolvimento da coróide e podem significar coleções remotas de células inflamatórias ou infecção subclínica.Universidade Federal de São Paulo (UNIFESP) Departamento de OftalmologiaUNIFESP Departamento de OftalmologiaUNIFESP, Depto. de OftalmologiaUNIFESP, Depto. de OftalmologiaSciEL

Abreu, Mariza Toledo

Amaro, Miguel Hage

Belfort, Rubens Junior

Muccioli, Cristina

Arquivos Brasileiros de Oftalmologia

Miguel Hage Amaro

Cristina Muccioli

Mariza Toledo Abreu

Rubens Belfort Jr.

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Remote hypofluorescent dots in recurrent ocular toxoplasmosis on indocyanine green angiography

Repositório Institucional UNIFESP

Arq Bras Oftalmol. 2007;70(6):901-4Pontos hipofluorescentes remotos em toxoplasmose ocular recorrente naangiografia com indocianina verdeStudy conducted at the Department of Ophthalmologyof Universidade Federal de São Paulo - UNIFESP - SãoPaulo (SP) - Brasil.1 Oftalmologista do Departamento de Oftalmologia daUniversidade Federal de São Paulo - UNIFESP - SãoPaulo (SP) - Brasil.2 Professora Livre Docente do Departamento de Oftal-mologia da UNIFESP - São Paulo (SP) - Brasil.3 Professora Adjunto do Departamento de Oftalmologiada UNIFESP - São Paulo (SP) - Brasil.4 Professor Titular do Departamento de Oftalmologia daUNIFESP - São Paulo (SP) - Brasil.Corresponding author: Miguel Hage Amaro.  Rua Quin-tino Bocaiuva, 516 - Belém (PA) CEP 66053-240E-mail: amaro@amazon.com.brRecebido para publicação em 13.07.2005Última versão revisada em 24.03.2007Aprovação em 03.09.2007Miguel Hage Amaro1Cristina Muccioli2Mariza Toledo Abreu3Rubens Belfort Jr.4Remote hypofluorescent dots in recurrent oculartoxoplasmosis on indocyanine green angiographyINTRODUCTIONToxoplasmosis is a common disease that occurs worldwide in birds andwarm-blooded mammals including humans(1). It is caused by infection of asingle-celled parasite called Toxoplasma gondii(1).Toxoplasma gondii infection is a frequent cause of uveitis(1-5). Toxo-plasma gondii is an obligate intracellular parasite and infection is wides-pread in nature.Human toxoplasmosis may occur in either a congenital or an ac-quired form. Serologic evidence of previous Toxoplasma gondii infec-tion is present in 20% to 70% of the population of the United States ofAmerica(6-7).Toxoplasma gondii is a coccidian classified as belonging to the phylumApicomplexa, class Sporozoa, order Eucoccidia and suborder Eimeria. Theinfection is a zoonosis and members of the cat family are the definitive hosts(8-17).Acute systemic toxoplasmosis in normal hosts is most often a subcli-nical infection but may present as a mild flu-like illness. The disease iscontrolled by the host’s immune response to the acute infection. If theparasite reaches the eye, a focus of infection is established, which progres-ses from mainly a retinitis with some spillover inflammation into theadjacent choroid and vitreous(1).It is estimated that about two-thirds of patients with toxoplasmosis haverecurrent episodes of inflammation(18). Various mechanisms have beenhypothesized as the cause of recurrent inflammatory episodes including: (1)Keywords: Toxoplasmosis, ocular/diagnosis; Choroiditis; Fluorescein angiography; Indo-cyanine green/diagnostic use; Retinitis; RecurrencePurpose: To report the findings of indocyanine green angiographyperformed in patients with recurrent ocular toxoplasmosis. Methods:Institutional prospective analysis of 23 eyes from 23 immunocompetentpatients with recurrent ocular toxoplasmosis aged between 17 and 41years. These patients underwent a complete ocular examination includingindocyanine green angiography. Results: Multiple hypofluorescentspots distant from the recurrent active lesion of retinochoroidal toxo-plasmosis were found in 26.08% of the patients. We also found multiplehypofluorescent satellite dots in 69.56% of the patients. Conclusion:These remote dots seen suggest either a more widespread choroidalinvolvement in this disease and this can represent simply remote collectionsof inflammatory cells or subclinical infection.ABSTRACT70(6)24.pmd 18/12/2007, 21:24901Arq Bras Oftalmol. 2007;70(6):901-4902 Remote hypofluorescent dots in recurrent ocular toxoplasmosis on indocyanine green angiographyreactivation of Toxoplasma gondii cysts within the retina; (2) anautoimmune response to remaining retinal antigen; and (3) rein-fection with live organisms. The first two mechanisms are sup-ported by the observation that recurrent lesions frequently de-velop at the borders of old retinochoroidal scars(18).Indocyanine green angiography (ICG) has been used to studyinflammatory chorioretinal diseases(19-20) and toxoplasmosis(21-23).In toxoplamosis, recurrent active retinal lesions on fluo-rescein angiography present hypofluorescence in the centerand staining of the dye on the edge of the lesions of acuterecurrent active retinitis(2).On indocyanine green angiography, recurrent active reti-nal lesions are hypofluorescent in all phases of the study.Satellite dark dots have been described around the hypofluo-rescent recurrent active lesion(21).We analyzed a case series of patients with recurrent oculartoxoplasmosis using ICG angiographic studies and sought topresent the respective findings in this study.METHODSThis is an Institutional prospective study. The studyprotocol was approved by the Medical Research Ethics Com-mitee of Universidade Federal de São Paulo (Escola Paulistade Medicina). We evaluated 23 eyes of 23 immunocompetentpatients, between January 2001 and June 2004. There were 10females and 13 males with age ranging from 17 to 41 years,with a mean age of 29. All patients had unilateral recurrenttoxoplasmic retinitis, at the time of diagnosis.Presentation of recurrent retinitis was classified in the mo-ment the patients were diagnosed(23). According to this classi-fication, the presentation of recurrent retinitis can be one of thefollowing: (1) large destructive lesions (in which active retinitisinvolves an area usually larger than the optic nerve head); (2)punctate inner retinal lesions (gray area of active retinitis withminimal edema and vitreous reaction) and; (3) punctuate outerretinal lesions. The patients underwent an ocular examinationincluding fluorescein angiography and indocyanine green an-giography, focusing on the  recurrent active retinal lesion, thesurrounding area and other areas in the ocular fundus. These testswere performed at the time of diagnosis; with the improvement ofinflammation and; after healing of the recurrent active lesion. Allpatients were treated for six weeks with oral antitoxoplasmicdrugs, such as sulfadiazine and pyrimethamine, and folinic acid.Oral prednisone 20 mg/day was also administered in half of thepatients if they presented vitreous inflammation, or if therecurrent lesion was located in the posterior pole of the eye, closeto the macular region.RESULTSFluorescein angiography showed hypofluorescence in thecenter and staining of the dye on the edge of the retinalrecurrent active lesion in all patients.ICG angiography showed multiple hypofluorescent dotssurrounding the active lesions in 70% of the eyes (Figure 1).In 26% of the eyes (six patients) hypofluorescent dots (Figu-res 2 and 3) were also seen in areas of the fundus distant fromthe active recurrent lesion and in areas of retina that appea-red normal on fundoscopy and fluorescein angiography atthe moment of the diagnosis.They are noticed in all the three morphologic variationsof retinitis presentation. The remote dots were found in sixpatients and three of them were treated with antitoxoplasmicdrugs plus steroid and the other three patients were treatedwith antitoxoplasmic drugs alone. Both the adjacent andremote hypofluorescent spots disappeared after treatmentand control of the active inflammation.DISCUSSIONResearchers agree that patients have a life-long risk ofrecurrences. A steady rise in the cumulative prevalence ofpatients who have had disease recurrences(24) was demons-trated. However, other authors(23) found that the frequency ofrecurrence drops in many patients after a few years, and thatthey eventually cease to occur. This decline in the frequencyof recurrences could be related to host factors, either invol-ving sequestration of tissue cysts or improved immunologi-cal control of infection. The latter possibility is unlikely,however, in view of the fact that immune defenses are belie-ved to decline with age. As a result, ocular diseases mayactually be more severe in older patients. Another possibi-lity is that tissue cysts have a finite lifespan in human hosts,and that patients will eventually have no tissue cysts thatcould reactivate. It is unlikely that this pattern of recurren-ces is the result of therapy, since there has been no demons-trable effect of short-term treatment on the intervals to firstrecurrences.A study(23) suggested that recurrences can develop inclusters, and that there can be long intervals between clus-ters. A theory(18) for this is that the clustering effect might beexplained by the fact that, with a given recurrence, the localnumber of tissue cysts increases through proliferation oforganisms during the active phase of disease, thereby increa-sing the likelihood that at least one tissue cyst will subse-quently reactivate. The risk of recurrences would again dropover time, as tissue cysts became nonviable; eventually,some disorder of host defenses would allow another episodeif any viable tissue remained in the retina, then the numberof tissue cysts would increase again, thereby initiating ano-ther cycle of frequent recurrences.In conclusion, our study shows intriguing findings whenobserving the results of ICG angiography in a case series ofrecurrent ocular toxoplasmosis, despite the fact that multiplehypofluorescent dots have been previously seen in inflam-matory chorioretinal diseases(19-20). In ocular toxoplasmosisthe most common finding is the occurrence of hypofluores-70(6)24.pmd 18/12/2007, 21:24902Arq Bras Oftalmol. 2007;70(6):901-4 903Remote hypofluorescent dots in recurrent ocular toxoplasmosis on indocyanine green angiographycent dots surrounding the active lesions called satellite darkdots, which were seen in approximately 75% of the cases in asmall case series(21-25). It was hypothesized that these hypofluo-rescent dots represent additional areas of infection becausethey progressed to white lesion in two cases(26). We also foundhypofluorescent dots around the active lesions. In addition,Figure 1- A) Nasal recurrent active toxoplasmosis; B) Satellite dark dotsA BA B CFigure 2 - A) Nasal recurrent active toxoplasmosis; B) Satellite dark dots; C) Remote dots temporal to the macula (marked by the arrowhead)Figure 3 - A) Juxtamacular recurrent active toxoplasmosis; B) Remote dots in the nasal region (marked by the arrowhead)A B70(6)24.pmd 18/12/2007, 21:24903Arq Bras Oftalmol. 2007;70(6):901-4904 Remote hypofluorescent dots in recurrent ocular toxoplasmosis on indocyanine green angiographyhowever, there were hypofluorescent dots distant from activerecurrent lesions in areas that appeared normal on fundoscopyand fluorescein angiography. These remote dots were seen in26% of the eyes in our case series.CONCLUSIONThe presence of these remote dots suggests either a morewidespread infectious disease than suspected or perhaps juststerile choroidal inflammation as a general response to intra-ocular inflammation. We believe that ICG angiography al-lowed us to observe results in cases of recurrent ocular to-xoplasmosis that had not been previously observed. Howe-ver, further studies will be necessary to elucidate the signifi-cance of these hypofluorescent remote dots.RESUMOObjetivos: Relatar os achados da angiografia com indocia-nina verde, realizados em pacientes com recidiva de toxo-plasmose ocular. Métodos: Análise institucional e prospec-tiva de 23 olhos de 23 pacientes, imunocompetentes comidades entre 17 e 41 anos. Estes pacientes foram submetidos aexame oftalmológico de rotina e a angiografia com indocia-nina verde. Resultados: Foram encontrados múltiplos pontoshipofluorescentes distantes da lesão ativa recidivada da to-xoplasmose retino-coroidiana em 26,08% dos casos, chama-dos por nós de pontos remotos e encontramos também, pon-tos hipofluorescentes circundando ou próximos da lesão ati-va recidivada em 69,56% dos casos. Conclusão: Os pontoshipofluorescentes distantes da lesão ativa recidivada, chama-dos de pontos remotos, não descritos previamente na doença,demonstram um maior envolvimento da coróide e podemsignificar coleções remotas de células inflamatórias ou infec-ção subclínica.Descritores:Toxoplasmose ocular/diagnóstico; Coroidite;Angiofluoresceinografia; Verde de indocianina/uso diagnós-tico; Retinite; Recidiva  REFERENCES1. Perkins ES. Ocular Toxoplasmosis. Br J Ophthalmol. 1973;57(1):1-17.2. Gass JD. Stereoscopic atlas of macular diseases: diagnosis and treatment. 2nded. St. Louis: Mosby; 1987.3. Schlaegel Jr TF. Toxoplasmosis. In: Duane TD, Jaeger EA, editors. Clinicalophthalmology. Hagerstown, MD: Harper & Row; 1978. vol.4.4. Tabbara KF. Toxoplasmosis. In: Duane TD, Jaeger EA, editors. Clinicalophthalmology. Hagerstown, MD: Harper & Row; 1978. vol.4. 5. Wilder HC. Toxoplasma chorioretinitis in adults. AMA Arch Ophthalmol.1952;48(2):127-36.6. Anderson S. Toxoplasma gondii. In: Mandell GL, Douglas RG Jr, BennettJE, editors. Principles and practice of infectious diseases. New York: JohnWiley; l979.7. McCabe RE, Remington JS. Toxoplasma gondii. In: Mandell GL, DouglasRG Jr. Bennett JE, editors. Principles and practice of infectious diseases, 2nded. New York: John Wiley; 1985.8. Cohen SN. Toxoplasmosis in patients receiving immunosuppressive therapy.JAMA. 1970;211(4):657-60.9. Couvreur J, Desmonts G. Congenital and maternal toxoplasmosis. A reviewof 300 congenital cases. Dev Med Child Neurol. 1962;4:519-30.10. Hoerni B, Vallat M, Durand M, Pesme D. Ocular toxoplasmosis and Hod-gkin’s disease: report of two cases. Arch Ophthalmol. 1978;96(1):62-3.11. Nicholson DH, Wolchok EB. Ocular toxoplasmosis in an adult receivinglong-term corticosteroid therapy. Arch Ophthalmol. 1976;94(2);248-54.12. Reynolds ES, Walls KW, Pfeiffer RI. Generalized toxoplasmosis followingrenal transplantation. Report of a case. Arch Intern Med. 1966;118(4):401-5.13. Ruskin J, Remington JS. Toxoplasmosis in the compromised host. AnnIntern Med. 1976;84(2):193-9. Review.14. Krick JA, Remington JS. Toxoplasmosis in the adult an overview. N Engl JMed. 1978;298(10):550-3.15. Miller NL, Frenkel JK, Dubey JP. Oral infections with Toxoplasma cysts andoocvsts in felines, other mammals, and in birds. J Parasitol. 1972;58(5):928-37.16. Swartzberg JE, Remington JS. Transmission of Toxoplasma. Am J DisChild. 1975;129(7):777-9.17. Teutsch SM, Juranek DD, Sulzer A, Dubey JP, Sikes RK. Epidemic toxo-plasmosis associated with infected cats. N Engl J Med. 1979;300(13):695-9.18. Holland GN. Ocular toxoplasmosis: a global reassessment. Part I: epidemio-logy and course of disease. Am J Ophthalmol. 2003;136(6):973-88.19. Slakter JS, Giovannini A. Multifocal choroiditis and the presumed ocularhistoplasmosis syndrome. In: Yannuzzi LA, Flower RW, Slakter JS. Indocy-anine green angiography. St Louis: Mosby; 1997. p.271-8.20. Slakter JS, Giovannini A, Yannuzzi LA, Scassellati-Sforzolini B, Guyer DR,Sorenson JA, et al. Indocyanine green angiography of multifocal choroiditis.Ophthalmology. 1997;104(11):1813-9.21. Auer C, Bernasconi O, Herbort CP. Toxoplasmic retinochoroiditis: new insi-ghts provided by indocyanine green angiography. Am J Ophthalmol. 1997;123(1):131-3.22. Da Mata AP, Orefice F. Toxoplasmosis. In: Foster S, Vitale A. Diagnosisand treatment of uveitis. Philadelphia: Saunders; 2002. p.385-410.23. Friedmann CT, Knox DL. Variations in recurrent active toxoplasmic retino-choroiditis. Arch Ophthalmol. 1969;81(4):481-93.24. Bosch-Driessen LE, Berendschot TT, Okngkosuwito JV, Rothova A. Oculartoxoplasmosis: clinical features and prognosis of 154 patients. Ophthalmolo-gy. 2002;109(5):869-78.25. Auer C, Bernasconi O, Herbort CP. Indocyanine green angiographic featuresin toxoplasmic retinochoroiditis. Retina. 1999;19(1):22-9.26. Bernasconi O, Auer C, Herbort CP. Recurrent toxoplasmic retinochoroiditis.Significance of perilesional satellite dark dots: seen by indocyanine greenangiography. Ocul Immunol Inflamm. 1997;5(3):207-11.70(6)24.pmd 18/12/2007, 21:24904

Pontos hipofluorescentes remotos em toxoplasmose ocular recorrente na angiografia com indocianina verde

https://doi.org/10.1590/s0004-27492007000600003

Pontos hipofluorescentes remotos em toxoplasmose ocular recorrente na angiografia com indocianina verde

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