British Journal of Ophthalmology, 1985, 69, 300-302

Schistosomotic choroiditis. II. Report of first caseJOSIt EYMARD HOMEM PITTELLA' AND FERNANDO ORItFICE2From the 'Division ofNeuropathology, Department ofPathology, and the 2Service of Uveitis,Federal University ofMinas Gerais Medical School, Belo Horizonte, Brazil

SUMMARY The first case of granulomatous choroiditis produced by Schistosoma mansoni withhistological confirmation is reported. The patient had the hepatosplenic and cardiopulmonaryforms of the disease and presented with cerebral schistosomiasis. The funduscopic aspects of thelesion and the possible pathways taken by the parasite to reach the choroid are discussed.

Uncommon sites for infection by Schistosoma man-soni seem to be associated with certain anatomico-clinical forms of the disease. One of these unusualsites, the brain, was recorded in 26% of patients withthe hepatosplenic form of schistosomiasis.' One casehas been reported of infection of the eye by animmature male S. mansoni parasite, in the anteriorchamber.2The funduscopic observation made by Orefice et

al.3 of choroidal nodules in five cases of the hepato-splenic form of schistosomiasis prompted one of theauthors (Pittella) to carry out a systematic search forova and granulomas in semiserial histological sectionsof the eyes of two deceased patients who had thehepatosplenic form of S. mansoni infection. In onecase S. mansoni ova and granulomas were found inthe choroid. We report this case, as no histologicallyconfirmed granulomatous choroidal schistosomoticinfection has been reported so far.

Case report

A female aged 17 years, born in Medina (MinasGerais State) and living in Belo Horizonte, had beenasymptomatic until 1½/2 years ago, when she pre-sented with dyspnoea on effort, which became worseover the next year or so. Recently she had sufferedsevere dyspnoea even at rest, with cough and vomit-ing. No palpitations or haemorrhagic sputum werenoted, nor thoracic or abdominal pain.On examination there was moderate tachydysp-

noea, cyanosis, and reduced capillary perfusion, butno oedema. The blood pressure was 140/80 mmHg,Correspondence to Dr Josd Eymard Homem Pittella, Departa-mento de Anatomia Patol6gica e Medicina Legal, Faculdade deMedicina da UFMG, Av. Alfredo Balena 190, 30.000-BeloHorizonte, Brasil.

the heart rate 108 per minute, with normal rhythm.The heart had a pulmonary presystolic click, with nor-mal first and second heart sounds. There was hepato-splenomegaly. Funduscopy was not done. The patientdied soon after hospital admission. The clinicaldiagnosis was severe pulmonary hypertension ofunknown origin (cardiopulmonary schistosomiasis?).

Pathological investigations showed a schistoso-motic type of Symmers hepatic fibrosis, a sclero-congestive spleen, a cardiopulmonary form ofschistosomiasis, and moderate ascites. An interatrialcommunication was found, with patent foramenovale, 0-4 cm diameter. Neuroschistosomiasis waspresent, with perivascular S. mansoni ova and mono-nuclear inflammatory infiltrate, a variable glialreaction, and occasional necrotic-exudative granu-lomas in the leptomeninges, cerebral cortex, andsubcortical right frontal and temporal white matter,the left putamen, and close to the left dentatenucleus. Calcified S. mansoni ova agglomerates werepresent in the left lateral globus pallidus, adjacent toa small lenticulostriate artery. There were slightcerebral oedema, a small cavum septi pellucidi, and apineal gland cyst. Anatomical variation of the circleof Willis was noted.

EYE EXAMINATIONNo changes were noted macroscopically on theinternal surface of the eye. Semiserial haematoxylin-eosin stained histological sections (7 lIm) showedthree schistosomotic granulomas characterised byembryonic and non-embryonic S. mansoni ova in thechoroid, projecting slightly into the retina, surroundedby epithelioid cells in palisade formation and moreexternal lymphocytes, plasmocytes, and eosinophilicgranulocytes. The largest granuloma also showedperiovular necrosis as a homogeneous acidophilic

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Schistosomoticchoroiditis. II. Report offirst case

Fig. 3 Schistosomoticgranuloma in theproductivephasein the choroid. Note S. mansoni ovum shell (arrow).Haematoxylin and eosin, x256).

Fig. 1 Schistosomoticgranuloma in the necrotic-exudativephase in the choroid. (Haematoxylin and eosin, x 100).

area (granuloma in the necrotic-exudative phase),which was absent in the other two granulomas-inthe productive phase (Figs. 1, 2, 3).

Discussion

The finding of schistosomotic granulomas in thechoroid of a patient with hepatosplenic schistosomia-sis mansoni confirms the suggestion made by Orefice4of choroiditis caused by S. mansoni. These granu-lomas may correspond to those nodules seen atfunduscopy by Orefice et al.3 One of the most

Fig. 2 Highermagnification ofFig. 1. (Haematoxylin andeosin, x256).

important morphological characteristics of thenodules is their variation in size, which may becorrelated with different phases in their develop-ment, as was noted in our case. As in the present casethe patients studied by Orefice et al.3 presented withhepatosplenic schistosomiasis and, with one excep-tion, the cardiopulmonary form. Another point to bementioned is the finding of S. mansoni ova in thebrain. Cerebral parasitism in schistosomiasis man-soni is found in 26% of patients with the hepato-splenic form '; most of these cases also presented withthe cardiopulmonary form of the disease.The possible pathways by which ova might arrive at

the choroid are worth considering. The discussion inPittella and Lana-Peixoto' on cerebral schistosomia-sis is pertinent. There are two possibilities: embolismof ova through the arterial or retrograde venoussystems, and local laying of ova following anomalousparasite migration. Arterial embolism requires thepresence of pre-existing pulmonary arteriovenousshunts56 or shunts related to the parasitism.78 How-ever, vascular changes in pulmonary schistosomiasiswhich were interpreted as arteriovenous fistulae areat present considered to result from the organisationof thrombi in the pulmonary arterial circulation.6Two alternative routes for arterial ova embolism tothe choroid are the porto-pulmonary azygous anasto-mosis,9 "' favoured by the portal hypertension in ourreported case, or the passage of ova to the systemiccirculation through direct communication betweenthe right and left heart, which was found in ourcase.On the other hand ova might arrive at the choroid

by retrograde venous routes through anastomosisbetween the ophthalmic vein, the cavernous sinus,cerebral veins, the spinal cord, and the portal systemby means of the vertebral venous plexus of Batson."

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The increase in flow due to portal hypertensionwould favour the spreading of ova by this route. 2Ova lying in the choroid following anomalous

parasite migration in the venous circulation can bepostulated after the finding of a pair of ova of S.haematobium in the orbital vein of a 12-year-oldchild'3 and ova agglomerates at a similar site in casesof conjunctival and lacrimal gland bilharzia.'"'5 Inour case an agglomerate of ova was found in theglobus pallidus, a finding already noted in other partsof the brain and spinal cord in cases of schistosomiasismansoni, ""s haematobium,'92" and japonica.2-23Similarly, adult parasites have been found in thecentral nervous system in a few cases.7224 Finally,another possibility by which ocular S. mansoniinfection may occur is the entry of cercariae throughthe conjunctiva and a posterior local parasite matur-ing.2 1325 However, in experimental models Queiroz,26Abboud et al.,27 and Lester and Freeman28 showedthat ocular entry of the parasite is not responsible forunusual eye lesions, resulting only in hepatointestinalschistosomiasis.

The authors thank Dr C J Simal for reviewing part of the literatureconsulted in this paper.

References

I Pittella JEH, Lana-Peixoto MA. Brain involvement in hepato-splenic schistosomiasis mansoni. Brain 1981; 104: 621-32.

2 Newton JC, Kanchanaranya C, Previte LR Jr. IntraocularSchistosoma mansoni. Am J Ophthalmol 1968; 65: 774-8.

3 Orefice F, Simal CJ, Pittella JEH. Schistosomotic choroiditis. I.Funduscopic changes and differential diagnosis. BrJ Ophthalmol1985; 69: 294-9.

4 Neves J, Pedroso ERP, Orefice F, et al. Esquistossomosepulmonar. III. Forma cr6nica extensa com hipertensao pul-monar e na vigencia de hipertensao portal associado a provavelcoroidite e retinite esquistossom6tica. Arq Bras Oftalmol 1978;41: 215-20.

5 Hayek H von. Die menschliche Lunge. 2nd ed. Berlin: Springer,1970: 302-6.

6 Spencer H. Pathology of the lung. 3rd ed. Oxford: PergamonPress, 1977: chapters 2, 10, and 16.

7 Barros OM, Giannoni FG, Marigo C, Frizzo FJ. Cor pulmonalee miocardite esquistossom6ticos. Consideraq6es clinico-

pathol6gicas a prop6sito de dois casos. Arq Hosp Santa Casa SPaulo 1956; 2: 33-72.

8 Faria JL. Pulmonary arteriovenous fistulas and arterial distribu-tion of eggs of Schistosoma mansoni. Am J Trop Med Hyg 1956;5: 860-2.

9 Calabresi P, Abelmann WH. Portocaval and portopulmonaryanastomoses in Laennec's cirrhosis and in heart failure. J CLinInvest 1957; 36: 1257-65.

10 Stein H, Stein S. Digital clubbing in cirrhosis of the liver. Lancet1961; ii: 999-1000.

11 Batson OV. The function of the vertebral veins and their role inthe spread of metastasis. Ann Surg 1940; 112: 138-49.

12 Faust EC. An inquiry into the ectopic lesions in schistosomiasis.Am J Trop Med Hyg 1948; 28: 175-9.

13 Badir G. Schistosomiasis of the conjunctiva. Br J Ophthalmol1946; 30: 215-21.

14 Welsh NH. Bilharzial conjunctivitis. Am J Ophthalmol 1968; 66:933-8.

15 Jakobiec FA, Gess L, Zimmerman LE. Granulomatous dacryo-adenitis caused by Schistosoma haematobium. Arch Ophthalmol1977; 95: 278-80.

16 Espin J. Mielitis producida por huevos de Schistosoma mansoni.Rev Policl Caracas 1941; 10: 245-59.

17 Aleman GC. Localizacion ectopica aparentemente asintomaticade huevos de Schistosoma mansoni en el encefalo. Reporte decuatro casos. Arch Hosp Vargas 1966; 8: 71-84.

18 Budzilovich GN, Most H, Feigin I. Pathogenesis and latency ofspinal cord schistosomiasis. Arch Pathol 1964; 77: 383-8.

19 Gelfand M. Schistosomiasis in South Central Africa. Cape Townand Johannesburg: Juta, 1950: 194-202.

20 Chitiyo ME. Schistosomal involvement of the choroid plexus.CentrAfr J Med 1972; 18: 45-7.

21 Greenfield JG, Pritchard B. Cerebral infection with Schisto-somiasis japonica. Brain 1937; 60: 361-72.

22 Chang TH, Smith GW, Riesenman FR, Alston EF. Cerebralgranuloma due to schistosomiasis. JAMA 1948; 136: 230-8.

23 Torres ML Jr. Cerebral schistosomiasis: clinical report of aproven cerebral granuloma and review of 41 other proven casesin the literature. Philipp J Surg Surgical Specialities 1965; 20:289-307.

24 Raper AB. Cerebral schistosomiasis. East Afr Med J 1948; 25:262-3.

25 Diamantis A. Les tactismes en bilharziose. C R Congr Int MedTrop Hyg (Cairo, 1928) 1932; 4: 797-816.

26 Queiroz JM de. Aspectos experimentais e clinicos das manifes-taq6es oculares da esquistossomose mansoni. Ophthalmol lberoAmericana 1961; 22: 115-78.

27 Abboud IA, Hanna LS, Ragab HAA. Experimental ocularschistosomiasis. Br J Ophthalmol 1971; 55: 106-15.

28 Lester RJG, Freeman RS. Eye penetration by cercariac ofSchistosoma mansoni. J Parasitol 1975; 61: 970-2.

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