Brit. J. Ophthal. (1976) 6o, 365

Ocular toxocariasis in adults

E. R. RAISTRICK AND J. C. DEAN HARTFrom the Department of Ophthalmology, Bristol Eye Hospital, Bristol

The larva of the nematode Toxocara canis wasfirst identified as a cause of intraocular disease byNichols (1956). Subsequent studies showed that itmay produce a variety of ocular lesions, includinglocalized retinal granulomata (Ashton, I960),endophthalmitis (Irvine and Irvine, 1959; Duguid,i96ia), or papillitis (Bird, Smith, and Curtin,1970). Nearly all the reported cases are of ocularlesions in children (Wilkinson and Welch, 1971),and the inference has been that the unhygienichabits of infants coming into contact with infecteddogs, or soil contaminated with the ova of thenematode, is a major factor in limiting oculardisease to the young (Duguid, i96ib; Unsworth,Fox, Rosenthal, and Shelton, I965). However, theproportion of the population with antibodies toToxocara species increases with age. In a study ofhealthy blood donors in the age group i8-25 yearstoxocaral fluorescent antibody tests were positivein 4-5 per cent and this figure rose to 7 I per centin the 30-40 age group (Woodruff, 1973). Clearlyadult toxocaral infection also occurs.

Clinical reports of retinal lesions in adults dueto presumed toxocaral infection are few. Phillipsand MacKenzie (I973) described the case of a25-year-old woman who presented with a historyof recent uniocular visual deterioration and wasfound to have a right papillitis. Initial toxocaralfluorescent antibody tests were negative, but laterthey were positive. More recently, another casewas reported of a so-year-old man who developedmoderate deterioration of vision in his right eyeafter a short febrile illness. He had a right pigmentepithelial detachment adjacent to the maculaand a linear opacity in the centre of the lesionchanged its orientation over a period of days. Hehad a transient eosinophilia and toxocaral fluores-cent antibody tests were positive (Raistrick andDean Hart, I975).

In this paper the ocular findings in three patientsin the age group 20-29 years who complained ofrelatively sudden uniocular visual loss are described.All had posterior polar retinal lesions in theaffected eyes, and ophthalmoscopic findings closely

Address for reprints: Mr J. C. Dean Hart, Bristol Eye Hospital,Bristol BSI 2LX

resembled those of proved toxocaral granulomatain children (Ashton, I960). In all cases the toxocaralfluorescent antibody tests were positive.

Case reports

CASE I

A 20-year-old woman secretary with a record ofgood health complained in June I972 of deterioratingvision in the left eye over a period of four weeks andintermittent, left-sided frontal headaches. Her correctedvisual acuities were 6/5 right and less than 6/6o left.The right eye was normal on biomicroscopy andophthalmoscopy, but in the fundus of the left eye therewas a raised pigmented lesion involving the macula.Near to it were a few small, deep retinal haemorrhagesand the surrounding retina appeared oedematous(Fig. ia). There was a dense central scotoma of theleft eye. X-ray examination of chest and skull showedno abnormalities and an ESR, a full blood count, and adye test for toxoplasma were all within normal limits.No diagnosis was made and therefore no treatmentinstituted. Five months later the vision had improvedspontaneously to 6/12 in the affected eye, though theretinal lesion appeared to be somewhat more extensive.

In January I973 the left vision had fallen to 6/i8 andthe patient was admitted to hospital for further assess-ment. A general physical examination showed no posi-tive findings. A short trial of systemic corticosteroidtherapy failed to ameliorate her symptoms and hervision continued to deteriorate. Some nine monthslater the left acuity was reduced to counting fingersand the lesion now appeared as a raised white opaque,umbilicated swelling with clearly defined edges. Apreviously noted retinal blood vessel that crossed overthe margin of the mass and dipped into the depressedcentral area had become grossly dilated (Fig. ib). Asthe lesion on ophthalmoscopic examination closelyresembled an illustration of toxocaral granuloma in achild described by Ashton (I960) we performed atoxocaral fluorescent antibody test. This was positive.On subsequent questioning the patient admitted closecontact with a dog a few months before the onset ofthe symptoms.

In November 1974 the retinal lesion had flattenedsomewhat and the engorged blood vessel retumed toits original calibre (Fig. ic). Six months later the patient'scentral vision remained grossly impaired, but thelesion involving the macula was much flatter. Surround-ing pigmentary changes were now obvious. Seven

366 British Journal of Ophthalmology

(a) (b)

(c)

months afterwards there was retinal scarring involvingthe macula with further progression of pigmentarydisturbances at the posterior pole (Fig. id).

Fluorescein angiographyFluorescein angiography soon after the patient was

first seen showed, in the initial part of the dye transit,masking of the choroidal fluorescence at the site of thepigmented lesion with no abnormality of the overlyingretinal vessels. In the venous and late phases there was

progressive uptake of dye in the central area of themass (Fig. za, b, c). Angiograms repeated in December1975 showed changes associated with pigment epithelial

FIG. 2 Case i. Left retinal fluorescein angiogramsequence on presentation. (a) Early arterial phase.(b) Venous phase. (c) Residual phase. Initial choroidalmasking of region occupied by lesion and subsequentleakage of fluorescein dye at site of mass

clumping and atrophy localized to the posterior pole(Fig. 3a, b) with minimal uptake or leakage of dye.

CASE 2

A 25-year-old man, a driver, was referred in August1973 with a few weeks' history of intermittent right-sided frontal headaches, occurring mostly in the even-ings, and a progressive loss of central vision in hisright eye. There was no history of general symptomsand his medical history was unremarkable. His leftvisual acuity was 6/4 and the right was reduced tocounting fingers. The left eye showed no abnormalfeatures, but ophthalmoscopy of the right fundus

Ocular toxocariasis in adults 367

FIG. I Case I. Changes in appearance of left posterior polar lesion involving the macula. (a) On presentation.(b) After I5 months. (c) After 27 months. (d) After 40 months

showed gross swelling of the optic disc and a smallpigmented lesion on its temporal side (Fig. 4). Thesuperficial disc capillaries appeared engorged andretinal folding could be seen between the pigmentedmass and the disc. A papillitis or tumour involving theoptic nerve head was tentatively diagnosed and thepatient admitted to hospital for further investigations.

General physical and neurological examination wasnegative, as were the results of x-ray examination ofskull and optic foramina, carotid angiograms, and air

encephalograms. A full blood count and plasma viscosityestimation were within normal limits. A trial of systemiccorticosteroids produced no improvement in symptoms.When seen in January I974 the patient's visual statushad not altered. The disc, however, appeared lessswollen and the pigmented area temporal to the discwas more obvious and clearly defined. He had an eosino-philia of 8 per cent and a toxocaral fluorescent antibodytest proved positive. The patient denied recent contactwith dogs or puppies. Subsequent examinations at

368 British Journal of Ophthalmology

FIG. 4 Case 2. Viezw when patient presented of rightswollen disc and mass at 9 o'clock

(b)

FIG. 3 Case i. Left retinal fluorescein angiograms at40 months. (a) Early arterial phase. (b) Residualangiogram. Extensive retinal pigmentary disturbancesare now an obvious feature, with minimal uptake or

leakage of dye in residual phase

six-monthly intervals showed a gradual decrease in discswelling and progressive pigmentation of the retinatemporally.

Fluorescein angiographyFluorography of the right retina in August I973 showeddilatation of the prepapillary capillary plexus andmasking of the choroid in the region of the pigmented

lesion in the early phase of the transit. In the residualphase there was profuse leakage of dye from the disccapillaries and uptake of fluorescein in the centre ofthe pigmented lesion (Fig. 5a, b). Fluorescein studiesin November 1975 showed that the dilated capillariesoverlying the disc were less prominent than before,with reduced leakage of dye from these vessels. Therewere extensive pigmentary disturbances in the area

around the retinal lesion described on presentationbut no leak or uptake of dye was recorded.

CASE 3

A 20-year-old bank clerk was seen at the BristolEye Hospital in November 1974 with a history ofgross impairment of left central vision of nine months'duration. Visual loss had been rapid. He had no othersymptoms and his health had been good. He hadinitially attended another eye unit, where retino-choroiditis had been diagnosed. It was first thoughtthat the retinal changes might be due to Histoplasmosiscapsulatum infection, but a histoplasmin test was

negative, as was a Mantoux test. A full blood countshowed nothing abnormal. On examination in Bristolhis right visual acuity was 6/6 and his left was handmovements. A large left central scotoma was plotted.No abnormalities were noted in the anterior segmentor vitreous of his left eye, but ophthalmoscopy showeda raised pale area involving the macula, with surroundingpigment changes and some small retinal haemorrhagesaround the periphery of the lesion (Fig. 6). No abnormalfeatures were found in the right eye. A toxocaral fluor-escent antibody test was positive. The patient admittedfrequent contact with a dog at his parents' home.When seen in October I974 his visual status remained

unaltered but the changes at the posterior pole covereda wider area with obvious retinal pigmentary distur-bances. Nine months later his visual acuity had not

(a)

Occular toxocariasis in adutlts 369

FIG. 6 Case 3. Left eye on presentation. View of paleraised lesion involving macula

(b)

FIG. 5 Case 2. Retinal fluorescein angiograms on

presentation. (a) Early venous phase. (b) Residualangiogram. Prepapillary capillary plexus dilated.Massive leakage of fluorescein dye from these vessels isprominent feature in residual angiogram

improved. Although the mass appeared flatter than on

presentation pigmentation of the retina continued to

progress.

Fluorescein angiographyRetinal fluorography on his first visit to the BristolEye Hospital showed early masking of the choroidalfluorescence in the left eye and a later uptake of dye in

the centre of the lesion as described in cases I and z.

Repeat angiograms in July I975 showed merely a

localized pigmentary disturbance without leak or

uptake of dye.

Discussion

The ophthalmoscopic appearances of toxocaralretinal granulomata at the posterior pole were

described in four children by Ashton (I960). He

reported retinal lesions which were solitary, pale,discrete, circular, and raised. Blood vessels promi-nent on the edge of the mass became lost from view

in the central area in two cases, and retinal haemor-

rhages adjacent to granulomata were reported in

two further cases. The initial retinal findings in

the adults reported in this series showed many of

the features mentioned by Ashton. Moreover, we

have followed the progressive nature of the retinallesion in case i for 3 - years from almost the initialto a late, less active stage. We believe that allthree cases show manifestations, on presentationand later, which fit into a definite clinical patternnot previously described in adults.On entering the systemic vascular circulation

the second stage toxocaral larva is washed alongin the blood stream until arrested in a vessel whosecalibre permits no further progress. The organism,a very active borer (Sprent, I954), then passes

through the vessel wall and takes up a positiondeep in the tissues, where it may remain alive for a

long time. We suggest that retinal haemorrhagesproduced by the passage of the larva throughthe vessel wall and sudden subsequent movementsof a foreign organism adjacent to the macula

(a)

370 British Yoturnal of Ophthalmology

could cause the initial retinal visual disturbances,and that as the parasite becomes less active retinalfunction may transiently improve, as in case i.

Eventually, however, the larva dies and disin-tegrates, prompting an intensified tissue responsewhich leads to focal disruption of the neural layersof the retina (Ashton, I960) and disturbances ofthe pigment epithelium. During this active inflam-matory stage increased vascularity in the regionof the mass might be expected, and the localvascular dilatation in cases i and 2 suggests that asimilar process could have happened in thesepatients. Later, as the cellular activity becomesreduced, flattening of the mass occurs, the vesselsreturn to their previous calibre, and disturbancesof the pigment epithelium promoted by the earlierinflammatory response appear more obvious andwidespread.The fluorescein studies in all cases showed initial

masking of the choroidal phase at the site of thepigmented lesion due to thickening or opacification,or both, of the overlying retina, and the localizedhyperfluorescence in the residual phase probablyresulted from uptake of dye into cystic spaces orstaining of inflammatory tissue. Later studiesshowed extensive pigmentary disturbances at theposterior pole with no leakage of fluorescein dye,corresponding to a less active phase of the diseaseprocess. In case 2 marked dilatation of the prepapil-lary capillary plexus was a prominent feature, andpossibly the process was fairly active when thepatient first presented. The initial ophthalmoscopychanges were similar to those in a case of nematodeoptic neuritis reported by Bird and others (1970).

Unilateral ocular pain or headache was a promi-nent symptom in two of our patients. Severeretro-ocular pain was completely relieved within24 hours by vigorously light-coagulating the sitepresumed to be occupied by a larva in a patientwho presented with evidence of toxocariasis(Raistrick and Dean Hart, 1975). Apparentlythe living organism may cause this symptom, since

ocular pain was also relieved after thiabendazinetreatment in a presumed case of ocular toxocaralinfection (Unsworth and others I965).The soil of many recreational areas in and around

towns and cities of the United Kingdom is heavilycontaminated with the live ova of toxocara. Borgand Woodruff (I973) found ova of Toxocaraspecies in 24-4 per cent of 8oo soil samples takenfrom public places. As such open spaces are usedfor picnics and sporting activities there is ampleopportunity for ova to enter the human body.Children of dog owners may no longer be assumedto be the only section of the community exposed tothis hazard, nor can the absence of a history ofcontact with animals that might harbour the para-site exclude the diagnosii>.Although histological verification of toxocaral

lesions involving the retinae of adults is lackingtoxocara larvae were probably alone responsiblefor the lesions in our patients, and this diagnosisshould be considered in adult patients presentingwith similar symptoms and signs.

SummaryHuman infection by toxocara larvae has beenthought to be predominantly a disease of youngchildren, but the percentage of the population withantibodies to this nematode worm has recentlybeen shown to increase with age. Although adefinite diagnosis of ocular toxocariasis can bemade only by identifying the larva histologically,the evidence in three cases presenting with recentuniocular loss of vision strongly suggests thatadults may also be affected. The lesions noted onophthalmoscopy closely resembled toxocaral granu-lomata in children. Toxocaral fluorescent antibodytests were positive in each case.

We thank Professor A. W. Woodruff for advice and hisstaff for performing the toxocaral fluorescent antibodytests. We thank Mr J. Morgan for photographic services,and Mrs M. Roach for her secretarial help.

References

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(I96Ib) Ibid., 45, 789IRVINE, W. c., and IRVINE, A. R. (1959) Amer. J. Ophthal., 47, I85NICHOLS, R. L. (1956) J. Parasit., 42, 349PHILLIPS, C. I., and MACKENZIE, A. D. (I973) Brit. med. J., I, I54RAISTRICK, E. R., and DEAN HART, J. C. (1975) Ibid., 3, 4I6SPRENT, J. F. A. (I954) Y. Parasit., 40, 6o8UNSWORTH, A. C., FOX, J. C., ROSENTHAL, E., and SHELTON, P. A. (I965) Amer. J. Ophthal., 6o, 127WILKINSON, C. P., and WELCH, R. B. (197I) Ibid., 71, 921WOODRUFF, A. W. (I973) Trans. roy. Soc. trop. Med. Hyg., 67, 755