Schistosomotic choroiditis. Funduscopicchanges anddifferential … · granuloma in the choroid of a patient with hepato-splenic schistosomiasis' confirms the hypothesis of Nevesetal.7

British Journal of Ophthalmology, 1985, 69, 294-299

Schistosomotic choroiditis.I. Funduscopic changes and differential diagnosisFERNANDO OR.tFICE,' CARLOS JORGE RODRIGUES SIMAL, ANDJOSI. EYMARD HOMEM PITTELLA2

From the 'Service of Uveitis and the 2Division ofNeuropathology, Federal University of Minas Gerais,Medical School, Belo Horizonte, Minas Gerais, Brazil

SUMMARY This paper presents the results of biomicroscopy and funduscopy on five patients withhepatosplenic schistosomiasis mansoni. Fluorescein angioretinography was performed on twopatients. All cases showed yellowish white multiple billateral nodules of various sizes, located inthe choroidal plane. The nature and differential diagnosis of these nodules is discussed, and thesuggestion is made that they represent cases of schistosomotic nodular choroiditis.

Schistosomiasis (Schistosoma mansoni, S. haemato-bium, and S. japonicum) is a worldwide public healthproblem, affecting approximately 200 millionpeople, with roughly 10 million cases in Brazil.' S.mansoni is the most widely distributed species,present in the Caribbean Isles, South America,Africa, and Arabia, with widespread geographicalextension and an increase in prevalence.2'3The S. mansoni hepatosplenic form of the disease

is both common and has serious consequences. InBrazil it affects 3 to 12% of patients with schisto-somiasis.4 I The parasite has unusual locations in thehepatosplenic form of the disease, with 26% of thepatients presenting with cerebral parasites.6During funduscopic examination of a child with

hepatosplenic schistosomiasis Orefice in 1968observed7 yellowish white nodules of various sizes inthe choroid in both eyes. This finding suggested thepossibility of involvement of the uveal tract, as incysticercosis. Further examinations of 50 patientswith hepatosplenic schistosomiasis revealed fourcases with similar choroidal changes.The recent finding of schistosomotic granulomas in

the choroid of a patient with hepatosplenic schisoto-somiasis8 confirms the impression that these oph-thalmic changes were caused by that disease, a con-dition not so far described.

Case reports

CASE 1 (Neves et al., 1978)7This case has been reported on by Neves et al.7 It is ofCorrespondence to Dr Fernando Or6fice, Rua Espirito Santo 1634,apto. 102, 30.000 Belo Horizonte, MG, Brazil.

a girl aged 9 years, white, admitted to hospital in1968.

Physical examination. Porta-caval type ofcollateralcirculation. Liver palpable at 4 cm below the costalmargin. Spleen palpable at 2 cm below the rightcostal margin and 8 cm under the xiphoid.

Laboratory tests. Stool examination showed viable

A B C

V. body Nodule

abFig.

1Drawing ofoptic section ofa nodule. The anterior

retina profile line (a') projects slightly towards the vitreousbody; there is discontinuity ofthe posterior retina profile line(b'). Translucent tissue is observed in the retina andchoroid. A=Internal limiting membrane. B=Pigmentepithelium. C= Sclera. a'=Anterior retina profile line.b'= Posterior retina profile line.

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Schistosomotic choroiditis. I. Funduscopic changes and differential diagnosis

Fig. 2 Case 1: rignt eye, witn multiple wnhitsn noaules, onearrowed.

S. mansoni ova. Mantoux test positive at 1:100000.Chest x ray showed disseminated micronodules inboth lungs and an increase in cardiac area. Electro-cardiogram showed right ventricular overload.Eye examination. Right eye, visual acuity 20/60

with no correction; left eye, 20/20. Intraocularpressure was 13 mmHg in both eyes. With theGoldmann-Busacca contact lens the vitreous bodyappeared free of inflammatory cells, even close tofundus lesions. An optic section of the nodules (Fig.1) showed a projection of the anterior profile of theretina towards the vitreous body, and discontinuity ofthe posterior profile of the retina, as evidence of thelack of pigmented retinal epithelium. Indirectbinocular ophthalmoscopy (Fig. 2, right eye) of botheyes disclosed the presence of numerous yellowishwhite translucent nodules of various sizes, distri-buted irregularly, but with some concentration closeto the optic nerve and blood vessels. The veins weremoderately engorged, and the maculae werenormal.

CASE 2A 14-year-old female, of mixed colour, was admittedto hospital in 1978.

Physical examination. Liver palpable at 12 cmbelow the costal margin on the hemiclavicular rightline and 16 cm below the xiphoid, with a blunt edge,not painful, with a micronodular surface. Spleenpalpable at 4 cm below the left costal margin on theleft hemiclavicular line, with a blunt edge, notpainful.

Laboratory tests. Tuberculin test was not reactive.

rig. - Lbase -:rignr eye, win wnit.sn meaium sizeu noauuesclose to the optic nerve; oneperifoveal nodule (arrow).

Stool examination showed viable S. mansoni ova.Electrocardiogram showed right ventricular over-load and diffuse ischaemia. An oesophagogramshowed oesophageal varices. A chest x ray showedenlarged heart, mainly the right ventricle; diffusemicronodules in both lungs. Haemodynamic testsshowed hypertension in right chambers and slighthypertension in left chambers. Hepatic biopsyshowed granulomas suggesting schistosomotic origin.Lung biopsy showed granulomas with S. mansoniova.Eye examination. Visual acuity in both eyes was

20/20. Intraocular pressure in both eyes was 15mmHg. Anterior chamber biomicroscopy showed noinflammatory cells. Vitreous body biomicroscopyshowed rare cells. With the Goldmann-Busaccacontact lens the vitreous body disclosed rare in-flammatory cells and occasional nodules with asimilar aspect to those in case 1. Indirect binocularophthalmoscopy of both eyes (Figs. 3 and 4, righteye) revealed yellowish white nodules ofvarious sizesdistributed irregularly, with greater concentrationaround the optic nerve in the right eye. Fluoresceinangioretinography of the right eye (Figs. 5 A and B,right eye) showed hyperfluorescent nodules in theposterior pole appearing in early phases, with noleakage in late phases. The left eye presented similarfindings.

CASE 3This was a man aged 35 years, of mixed colour,admitted to hospital in 1979. He had been treated forschistosomiasis with hycanthone five years before,

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6Fernando Orefice, Carlos Jorge Rodrigues Simal, and Jose EymardHomem Pittella

Fig. 4 Case2: right eye,compositefundus with greenfilter,showing nodule distribution(arrows).

when he presented with portal hypertension associ-ated with stools positive for S. mansoni.

Physical examination. No significant changes.Laboratory tests. The Mantoux test was positive at

1:10000. A brucella test was negative, and a histo-plasmin test negative. A chest x-ray was normal.Stool examination was negative.

Eye examination. Right eye visual acuity was 20/50with correction, left eye 20/20. The intraocularpressure was 13 mmHg in both eyes. Biomicroscopyof the anterior chamber and anterior vitreous body ofboth eyes revealed no inflammatory cells. Contactlens biomicroscopy was not done in this case. Indirectbinocular ophthalmoscopy (Fig. 6, right eye) of both

Fig. 5A Fig. 51Fig. 5 Case 2: A: right eye, fluorescein angioretinography (arteriovenous phase) showing hyperfluorescent nodules.B: nodules maintaining hyperfluorescence in laterphase ofthe examination.

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Fig. 6 Case3: right eye, with whitish medium sizednodules, and striation ofthe retinal internal limitingmembrane in the macular area (arrow).

eyes disclosed numerous yellowish white noduleswith irregular distribution. The macula in the righteye presented striations on the internal limitingretinal membrane. Fluorescein angioretinographywas not possible in this case.

CASE 4This case was a 16-year-old male, of mixed colour,admitted to hospital in 1981.

Physical examination. The spleen was enlarged(Boyd type III), towards the median line, hardened,not painful. The liver was not palpable. Cardiac andlung auscultation were normal.

Fig. 7 Case 4: right eye, aihaemorrhagic halo (arrow).

Laboratory tests. Stool examination was positivefor S. mansoni. A chest x-ray showed signs ofpulmonary hypertension and reduction in peripheralbase vascularity. Upper gastrointestinal bariumradiography showed oesophageal varices. Hepaticbiopsy showed granuloma of possible schistosomoticorigin.Eye examination. The visual acuity for both eyes

was 20/20. Intraocular pressure was 12 mmHg in botheyes. Biomicroscopy of the anterior chamber andanterior vitreous body revealed no inflammatorycells. Contact lens biomicroscopy was not done in thiscase. Indirect binocular ophthalmoscopy (Fig. 7,right eye) disclosed small, yellowish white translucentnodules in both eyes. The right eye showed a nodulesurrounded by a haemorrhagic halo. Fluoresceinangioretinography was not possible in this case.

CASE 5This case was a 24-year-old male, white, admitted tohospital in 1982.

Physical examination. The liver was 4 cm below thecostal margin, not painful.

Laboratory tests. Stool examination showed S.mansoni viable and non-viable ova. Oesophago-gastroduodenoscopy showed medium calibreoesophageal varices. A chest x-ray was normal.Eye examination. The visual acuity for both eyes

was 20/20. Intraocular pressure was 16 mmHg forboth eyes. Biomicroscopy of the anterior chamberand anterior vitreous body revealed no inflammatorysigns. With the Goldmann-Busacca contact lens noinflammatory cells were found in the vitreous body in

Fig. 8 Case 5: left eye,distributed nodules.

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Fernando Orefice, Carlos Jorge Rodrigues Simal, andJose EymardHomem Pittella

Fig. 9B

Fig. 9 Case 5: A: left eyefluorescein angioretinography(arterialphase) showing hyperfluorescent nodules, and darkhypofluorescent nodule (arrow) with hyperfluorescent halo.B: (arterial-venous phase) maintains similarfindings. C:(latephase) with hyperfluorescent nodule (arrow).Fluorescein angioretinography ofthe right eye was similar.

either eye. A section of the eye showed nodules (Fig.1) similar to those in case 1. Indirect binocular oph-thalmoscopy disclosed yellowish white nodules ofvarious sizes in both eyes, with irregular distributionand some concentration around the optic nerve andclose to blood vessels (Fig. 8, left eye). Fluoresceinangioretinography (Figs. 9A, B, C, left eye) of theleft eye showed hyperfluorescent nodules in thearterial phase, and a hypofluorescent point sur-rounded by a hyperfluorescent halo in the lowertemporal region. No change in hyperfluorescencewas observed in the early arteriovenous phase. In the

late phase the hypofluorescent point became hyper-fluorescent. At this point the vein projected towardsthe vitreous body. Fluorescein angioretinography ofthe right eye was similar.

Discussion

These cases suggest that funduscopic changes mayoccur fairly frequently in hepatosplenic schisto-somotic patients. Of 50 patients five were found tohave such changes. These were yellowish white trans-lucent nodules of various sizes located in the choroid,

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confirmed by optical section biomicroscopy andfluorescein angioretinography in three of them. In allfive eases the anterior segment was not affected, andonly case 2 presented a small number of cells in thevitreous body, demonstrating the choroidal locationof these lesions.

It was noted that nodules did not interfere withvisual acuity if the maculae was not affected. Onlycase 3 had macular nodules.A comparison of these funduscopic findings with

changes found in similar conditions is the aim of thispaper. Our work was hampered by the lack ofreported data, probably due to the fact that examina-tion of the fundus is not routine in patients withschisotosomiasis.

Studying a group of military recruits (18-19 yearsof age) who had contact with river water in thevicinity of Belo Horizonte during trainingmanoeuvers, Orefice and Brandao (unpublishedwork) noted that 78 of a total of 130 recruits elimi-nated S. mansoni ova. Clinical and laboratory exam-inations led to the diagnosis of 39 patients in the acutephase, 17 in the chronic phase, and 22 undefinedcases. All had a normal fundus on examination. Nopatients had the hepatosplenic form of the disease.Few ocular findings have been attributed to S.

mansoni.' Uveitis and vascular changes in the retinain patients with stools positive for S. mansoni havebeen described, suggesting a possible association. "'5Non-specific lesions such as retinal haemorrhage andsoft and hard exudates were observed in 60 patientswith hepatosplenic schistosomiasis, but we wereunable to correlate these findings because othersystemic changes were present.'6

Since no histopathological examinations werepossible in these cases, the fundus lesions have beenanalysed by the nature of the changes and the dif-ferential diagnosis from other pathological choroidallesions. The dimension and colour of the choroidalnodules are similar to S. mansoni ova granulomaspresent in other organs of patients with schistosomia-sis. We believe that the choroidal nodules are S.mansoni ova granuloma. The possible pathways bywhich S. mansoni eggs could reach the eye are dis-cussed in the second part of this paper.8The recent histological finding of a schistosomotic

granuloma in the choroid of a patient with hepato-splenic schistosomiasis' confirms the hypothesis ofNeves et al.7 Another posibility is that these nodulesare the morphological changes due to immuno-complex deposits similar to those found in renalglomeruli7 and the choroidal plexus"I and not aninflammatory reaction to S. mansoni ova. However,these mechanisms do not produce micronodularlesions visible on endoscopy.The fundus lesions we encountered show some

similarity to those that occur in chronic miliarytuberculosis. All cases were investigated for thispossibility with or without positive Mantoux tests.Clinical study and follow-up allowed us to establish S.mansoni as responsible for the fundus lesions.

NOTE. Busacca's terminology was used in biomicroscopy. 19

We thank Dr Renato Laender and Dr Giambatista Coscarelli forintravenous fluorescein angiography, and Mrs Claudia Lambert fordrawing the optic section of the nodule.

References

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2 McCully RM, Barron CV, Chccvcr AW. Schistosomiasis. In:Benfered CH, Connor DH, eds. Pathology oftropical and extra-ordinary diseases. Washington, DC: Armed Forces Institutc ofPathology, 1976: 2: 482-3.

3 Hoffman Jr D. Schistosomiasis research. The strategic plan. NewYork: Edna McConnell Clark Foundation, 1983: 105.

4 Coutinho.A, Domingues ALC. Esquistossomose mansoni. In:Dani R, Paula Castro L, Perez V, Arabehety JT, eds. Gastro-enterologia. Rio de Janeiro: Guanabara Koogan, 1978: 850.

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11 Andrade C. Esquistossomose. In: Andrade C, ed. Oftalmologicatropical (Sul-Americana). Rio de Janeiro: Rodrigues, Jornal doCorreio-Brasil, 1940: 93-101.

12 Machado NR. Esquistossomose mans6nica e oftalmologia (notaprevia). Ophthalmol Ibero Americana 1956; 18: 89.

13 Queiroz JM. Aspcctos experimentais e clinicos das mani-festa06es oculares da esquistossomose mansoni. OphthalmolIbero Americana 1961; 22: 115-226.

14 Massa MJ, Laurijs L, Wijns (Louvain). Lesions parasitaires de laretine chez une femme bantouc. Bull Soc Belge Ophtalmol 1964;137: 412-23.

15 Vedy J, Carrica A, Rivaud C, Chanut G, Graveline J. A proposd'un cas de retinite chez un bilharzien. Med Trop (Madr) 1979;39: 603-7.

16 Lemos E. Alteraq6es retinianas na esquistossomose hepato-esplenica. Rev Bras Oftalmol 1980; 39: 123-8.

17 Hoshino-Schimizu S, Brito T, Kanamura HY, et al. Humanschistosomiasis: Schistosoma mansoni antigen detection in renalglomeruli. Trans R Soc Trop Med Hyg 1976; 70: 492-6.

18 Queiroz AC. Les6es da plexo cor6ide nas esquistossomosemans6nica. Arq Neuro-Psiquiatria (Sao Paulo) 1981; 39: 317-20.

19 Busacca A. Le fond de l'oeil. In: Busacca A, ed. Manual debiomicroscopie oculaire. Paris: Doin, 1966: 286-323.

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Schistosomotic choroiditis. Funduscopicchanges anddifferential … · granuloma in the choroid of a patient with hepato-splenic schistosomiasis' confirms the hypothesis of Nevesetal.7