British Journal of Ophthalmology, 1987, 71, 396-401

Ocular larva migrants: a case reportROBERT W LYNESS,' OLIVIA E EARLEY,' WILLIAM C LOGAN,',AND DESMOND B ARCHER'

From the Departments of 'Pathology and 'Ophthalmology, the Queen's University of Belfast, Royal VictoriaHospital, Belfast BT12 6BA

SUMMARY A case of intraocular toxocara larva migrans occurring in a 12-year-old boy ispresented. Motility is inferred from the nature of multiple intraocular lesions observed. Possiblemechanisms preventing a conclusive immunological response to the organism are discussed.

Ocular toxocariasis continues to present the ophthal-mologist with a problem of diagnosis despiteimproved investigative tools. Several clinicalpatterns of presentation are recognised.' One ofthese, the motile chorioretinal nematode, has beendescribed following ophthalmoscopic visualization,"and inferred from the discovery of a subretinal tubeon histological examination of a presumed case ofocular toxocariasis.4 We present a case of oculartoxocariasis in a 12-year-old boy which purports todemonstrate the intraocular motility of the toxocaralarva and the nature of the various lesions caused byits passage. We relate the difficulty in achievingserological confirmation of ocular toxocariasis topeculiarities in the intraocular host-parasite relation-ship.

Case report

A 12-year-old boy first attended the ophthalmicoutpatient clinic of the Royal Victoria Hospital,Belfast, on 26 March 1985. He complained of a

disturbance of vision in his left eye, present forapproximately six weeks.Three weeks after the onset of symptoms the

patient found he was unable to see out of the left eye,and since then there had been no recovery of vision.

The affected eye was comfortable. There was no

history of injury, ocular inflammation, or discharge.Thre patient was in good health otherwise, though hesuffered from intermittent attacks of asthma whichwere treated with a salbutamol inhaler. The asthmaticattacks were precipitated occasionally by contactwith a pet rabbit. There was no obvious contact withdogs, cats, or farm animals. At the age of 6 years thepatient was admitted to hospital suffering from(_orrcsponidcncc to Dr R W Lyncss.

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febrile convulsions. No specific diagnosis was madeand convulsions have not recurred. There was nofamily history of any ocular or relevant systemicdisease.

EXAMINATIONAt the first examination, on 26 March 1985, the visualacuity of the unaided right eye was recorded as 6/4and that of the left eye as accurate projection of light.Examination of the right eye showed it to be structur-ally sound in all regards. The left eye was injected,and biomicroscopy revealed slight flare and someinflammatory cells in the anterior chamber. Pigmentdeposits on the anterior lens surface and posteriorsynechiae were present (Fig. 1). The intraocularpressure was 18 mmHg on the right and 24 mmHg onthe left. The left lens was clear, but immediatelybehind the lens there was a grey-white intraocularmembrane or mass associated with an array of dilatedvascular channels and pigment deposits. The ocularfundus could not be visualised.

Systemic examination was negative, with no evid-ence of regional or generalized lymphadenopathy,skin lesions, arthropathy or hepatosplenomegaly.The right visual field was normal (Goldmann

perimetry) but it was not possible to obtain a plot onthe left side. Electroretinography showed a normal Bwave amplitude on the right side, but recordings onthe left side were extinguished, even to a bright flash.Fluorescein angiography (Fig. 2) confirmed thepresence of numerous dilated shunt-like bloodvessels within the retrolenticular mass. These bloodvessels filled rapidly in the early phases of angio-graphy; the major channels remained competent,while the smaller vessels leaked dye, causing theretrolenticular mass to become hyperfluorescent bythe later angiographic frames. Some of the large

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397Ocular larva migrans: a case report

I

vFig. I tuomicroscopic view ofIrissnowingpuosnruorsynechiae and the vascular cyclitic membrane.

vessels remained non-perfused throughout the angio-graphic series, which was consistent with eitherthrombosis or the 'steal phenomenon' seen in tumourcirculations. The late phase angiograms showedleakage of dye at the superior iris, but there was no

evidence of rubeosis iridis.The white blood cell count was 6.5x 109/l and the

eosinophil polymorphonuclear count was 0-26x 1091lor 4% of the differential white cell count. Theerythrocyte sedimentation rate (ESR) was 33 mm inthe first hour. The blood alkaline phosphatase at 182ml/l; (considered raised in an adult but within normalrange for a child of 12 years of age) was the onlybiochemical finding. The Rose-Waaler test and sero-

logical tests for Rh factor and rheumatoid arthritisfactor (latex) were negative. Serological tests fortoxoplasmosis were negative. The toxocara antibodyenzyme linked immunosorbent assay (ELISA) testwas weakly positive (0-63 units: normal values0-0-50). Chromosome analysis showed no abnor-malities.X-ray examination of the chest showed nothing

unusual except for an abnormality of the pulmonaryconus, which was not considered significant. X-raysof the left orbit were normal, and there was no

evidence of intraocular calcification. Ultrasoundexamination identified a retrolenticular mass con-

sisting of a dense posterior cyclitic membrane and a

funnel shaped retinal detachment. CT scanning

showed a distinct abnormality of the left eye, theglobe appearing to be of increased attenuation, withan area of further increased attenuation noted

Fig. 2 Late phasefluorescein angiogram showing largevascular channels within retrolental membrane.

posterolaterally. The appearance of the CT scansuggested to the radiologist 'a malignant tumourwithin the globe which may have arisen from theretina'.

MANAGEMENTThe patient was followed up for four weeks, duringwhich time the visual acuity diminished to no percep-tion of light in the left eye and the intraocularpressure fell to 4 mmHg. In view of the loss of visualfunction, impending ocular hypotony, and thesuggestion of the presence of an intraocular tumouron CT scanning, enucleation of the left eye wascarried out on 30 April 1985.

PATHOLOGICAL FINDINGSThe globe was fixed in formalin prior to processingand embedding in wax. Macroscopically the left eyemeasured 23x23x22 mm and showed no grossexternal abnormality. The cut surface showed anapparently normal anterior chamber. A cycliticmembrane posterior to a normal lens with anadherent funnel shaped detachment of the retina waspresent.

Histological examination of serial sections showeda normal cornea, filtration angles, iris, and lens. Acyclitic membrane (Fig. 3) extended from one part ofthe ciliary body, posterior to the lens, to the contra-lateral aspect of the ciliary body. This membraneconsisted of three generations of inflammatorytissue. These showed resolved and resolving inflam-mation with fibrinous organisation and more recent

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Robert W Lyness, Olivia E Earley, William C Logan, and Desmond B Archer

Fig. 3 Histologicalsection ofwholeeyeshowingcycliticmembrane (M) andfunnelshaped detachment ofthe retina(R).

inflammation composed of loose, oedematous, sero-fibrinous material infiltrated mainly by eosinophilpolymorphonuclear leucocytes but including someneutrophil polymorphs, lymphocytes, and plasmacells. Large blood vessels were readily apparent. Themembrane extended over the inner aspect of theretina producing a tractional retinal detachment.The retina was well preserved in most areas, which

confirmed that the detachment was a recent occurr-ence. There were two foci (Fig. 4) of eosinophilicnecrosis with the features of the Splendore-Hoeppliphenomenon' situated in the outer retina. Noorganism or remnants of an organism were foundin either of these lesions. One lesion containedCharcot-Leyden crystals. Elsewhere in the posteriorretina there was perivascular chronic inflammatorycell infiltration.

The choroid contained foci (Fig. 5) of eosinophilicpolymorphonuclear inflammation. One of these focallesions showed a perforated Bruch's membranepartially damming back the eosinophils and necroticeosinophilic material to cause a dark staining area onthe choroidal aspect. Eosinophilic material exudedthrough Bruch's membrane, detaching the retinalpigment epithelium. No organism or remnants of anorganism was found in this lesion. The remainder ofthe choroid showed low grade chronic inflammationand a relative absence of eosinophils.

In the subretinal space four separate discretespheroidal coagula (Fig. 6) were found. Theseconsisted of relatively acellular hyaline materialcontaining pigment debris from the retinal pigmentepithelium. A few macrophages were seen on thesurfaces of these coagula. No organism or remnantsof an organism was found in any of these four lesions.On level 152 of the serial histological sections a

granuloma (Figs. 7 and 8) composed mainly oflymphocytes, plasma cells, macrophages, foreignbody type giant cells, and a few eosinophils was seenin the subretinal space. This lesion contained a larvaof Toxocara canis with characteristic morphologicaland structural features.6

Discussion

We have demonstrated eight lesions in this eyeassociated with ocular toxocariasis, raising thequestion of how many larvae were involved in theirproduction. It is our contention that only one larvarather than up to eight was involved, as only one larvawas found after serial sectioning of each of the otherseven lesions. There was evidence of sequential

Fig. 4 Histological section oftheouter retina showing an area ofeosinophilic necrosis (N) withfociofCharcot-Leyden crystals (C-L,arrowed). Also present is asubretinal coagulum (Coag).H and E, polarised light. x 52.

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Ocular larva migrans: a case report

Fig. 5 Histological section ofchoroid showing an eruptioncomposed mainly ofeosinophilsand detaching the overlying retinalpigment epithelium (RPE).H and E. x 52.

(rather than synchronous) inflammatory eventsgiving rise to several 'waves' of cyclitic membraneformation and chorioretinal lesions at differentstages of development or degeneration. Further-more, there was no indication of worm infestation ofthe fellow eye or systemically.The lesions we have described seem to represent

different stages of the immunological reaction by thehost to the parasite. The immediate reaction, sur-

rounding the larva, consists mainly of lymphocytes,macrophages, and a few eosinophils.7 In the sub-jacent choroid, eosinophilic polymorphonuclearleucocytes have accumulated and intensified the focalinflammatory response, eventually erupting throughBruch's membrane to attack the larva within thesubretinal space. This choroidal lesion is character-

ised by an area of eosinophilic necrosis, surroundedby viable eosinophils, which extrudes through a

perforated Bruch's membrane to elevate the overly-ing retinal pigment epithelium. The choroidaleruption appears to have resolved, giving rise to an

expended coagulum as seen in the subretinal spaceand possibly the Splendore-Hoeppli phenomena.

It is possible to plot the path (Fig. 9) taken by thelarva in the vitreous and subretinal space, deducingthe chronological order from the type and age of theeight lesions present in this case. The likely sequenceof events is that the larva entered the anteriorvitreous from a peripheral branch of the retinalartery, initiating the reaction that caused the cycliticmembrane. The topography of the blood vesselsidentified in the cyclitic membrane suggests that the

Fig. 6 Histological section ofasubretinal coagulum (Coag)surrounded by macrophages andremnants ofa choroidal eruption.Hand E. x 52.

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40()~~~~~RobertW Lyness, Olivia E Earley, William C Logan, and Desmond B Archer

a

Fig. 9 Drawing of the eye depicting the presumed path ofthe toxocara larva. (1) Entrance to vitreousfrom retinalcirculation. (2) Site ofcoagulum at point ofentry tosubretinal space. (3, 4, 5) Sites ofsubretinalcoagula. (6) SitesofSplendore-Hoeppli phenomenon. (7) Site ofchoroidaleruption. (8) Site ofsubretinal granuloma containing thetoxocara larva.

Fig.7 Histological section ofsubretinal granuloma (L),which includes a toxocara larva. H and E. x 57.

larva moved from one part of the ciliary body to a

contralateral site and then gained access to the

subretinal space. Within the subretinal space the

larva moved freely. Such motility of the toxocara

Fig. 8 Histological section ofsuibretinal granuloma showing a

toxocara larva (L) and a giant cell

(GC), Note the paucity of

eosinophils. H and E. x 52.

larva and presumed helminths within the eye hasbeen reported in experimental toxocariasis in theeyes of mice" and primates," by the presence of asubretinal tube in one case report,' and by clinicianson ophthalmoscopic examination.2'

This case is an example of the clinical dilemma ofdifferentiating between a malignant intraoculartumour and other benign intraocular lesions despitepossession of an array of sophisticated and sensitive

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Ocular larva migrans: a case report

diagnostic tests. Of particular interest is the relativelylow eosinophil polymorph count (0.26 x 10'1 or 4% ofWBC) in the peripheral blood (normal values inchildren 0-03-0-7x 10'Il)" and the barely positiveELISA titre for toxocara, when compared with thepronounced inflammatory reaction in the eye as seenon histological examination. There is no evidencethat this host (in common with the patients inprevious reports)'2 was immunologically compro-mised or deficient before or after clinical presenta-tion.

Previous reports'" support the contention in thiscase that the worm load in patients with oculartoxocariasis is low. This may result in an appropri-ately slight immunological response by the host.'The findings in our case strongly suggest that thelarva of toxocara can move away from an inflamma-tory response to its presence. It is probable that inthis process the parasite manipulates its antigenicprofile by shedding its 'coat' (glycocalyx)'" Thusresidual antigenic material continues to stimulate theinflammatory response while the parasite in a newguise moves elsewhere. A change of antigenic profileserves to prevent a concerted antibody response bythe host, as each change of surface antigens requiressynthesis of a new set of antibodies to combat them. IsA further factor in the host-parasite relationship

peculiar to the eye may be the immunologicalsurveillance of the subretinal space. The outer retinaand the subretinal region are nourished and servicedby the choroidal circulation. It would appear that theinitial response via the retinal circulation and thesubsequent choroidal reaction may be delayed orcurtailed by the inner and outer blood retinal barriersrespectively. The evidence from our case suggeststhat the response to the larva in the subretinal space isa granuloma closely followed by a choroidal eruptionconsisting predominantly of eosinophils, burstingthrough Bruch's membrane into the subretinal spacein a bid to attack the parasite before it moves on. Thisobviously works in some instances, as previous casereports have described the remnants of larvae insimilar isolated chorioretinal lesions.

This case appears to represent an intermediatestage between a solitary choroidoretinal lesion'2 andnematode endophthalmitis'7 in the destruction of aneye by the toxocara larva. The histopathologicalappearances show that the larva can defend itselfby moving within the subretinal space. It is alsosuggested that the response of the host is attenuated

by an inadequate immunological surveillance of thesubretinal space with inner and outer blood retinalbarriers obstructing a concerted immunologicalresponse to the organism. It is perhaps for thesereasons and the scant number of parasites that theeosinophil count and ELISA titre are so low despitethe presence and activity of the larva. Such a hypo-thesis suggests that an organism in the eye couldeasily give rise to a negative or dubious positive resulton examination of the peripheral blood. This situa-tion will lead to a continuation of the diagnosis of'choroidoretinitis' due to presumptive toxocariasis inclinical ophthalmic practice, despite the availabilityand use of sensitive serological tests.

References

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2 Parsons HE. Nematode chorioretinitis: report of a case withphotography of a viable worm. Arch Ophthalmol 1952; 47:799-800.

3 Rubin ML, Kaufman HE, Tierney JP. An intraretinalnematode. Ophthalmology (Rochester) 1968; 72: 855-66.

4 O'Connor PR. Visceral larva migrans of the eye. Subretinal tubeformation. Arch Ophthalmol 1972; 88: 526-9.

5 Garner A, Klintworth GK. Pathology of ocular disease. NewYork, Basel: Dekker, 1982: 364.

6 Nichols RL. The etiology of visceral larva migrans. J Parasitol1956; 42: 349.

7 Kayes SG, Oaks JA. Development of the granulomatousresponse in murine toxocariasis. Am J Pathol 1978; 93: 277-94.

8 Olson U. Ocular toxocariasis in mice: distribution of larvae andlesions. Int J Parasitol 1976; 6: 247-51.

9 Ghafoor SYA, Smith HV, Lee WR, et al. Experimental oculartoxocariasis: a mouse model. BrJ Ophthalmol 1984; 68: 89-96.

10 Watzke RC, Oaks JA, Folk JC. Toxocariasis infection of the eye.Correlation of clinical observations with developing pathology inthe primate model. Arch Ophthalmol 1984: 102: 282-91.

11 Orfanakis NG, Ostlund RE, Bishop CR, et al. Normal bloodleukocyte concentration values. Am J Clin Pathol 1970; 53: 647.

12 Ashton N. Toxocara canis and the eye. Br J Ophthalmol 196t);44:129-46.

13 Glickman LT, Schantz PM. Epidemiology and pathogenesis ofzoonotic toxocarisis. Epidemiol Rev 1981; 3: 23t)-5t).

14 Wiseman RA. Hepatomegaly and allergic responses inhelminthic infections transmitted from animals. Proc R Soc Med1969; 62: 1t)46-8.

15 Smith HV, Quinn R, Kusel JR. et al. Effects of temperature andantimetabolites on antibody binding to outer surface of secondstage Toxocara canis larvae. Mol Biochem Parasitol 1981; 4:183-93.

16 Rockey JH, Donnelly JJ, Stromberg BE. Immunopathology ofascarid infection of the eye. Arch Ophthalmol 1981; 99: 1831-4).

17 Duguid IM. Chronic endophthalmitis due to toxocara. Br JOphthalmol 1961; 45: 705-17.

Acceptedfor publication 14 July 1986.

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