British Journal of Ophthalmology, 1987, 71, 391-395

Intraocular pentastomiasis causing unilateralglaucomaYARON LANG,' HANNA GARZOZI,' ZVI EPSTEIN,' SUSAN BARKAY,'DANIEL GOLD,' AND JACOB LENGY'

From the 'Department of Ophthalmology, Central Emek Hospital, Afula, Israel, and the 2Departmetit ofHuman Microbiology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

SUMMARY We present a case of intraocular pentastomiasis in a 12-year-old Israel Arab boy. Asingle secondary pentastomid larva, most likely of Linguatula serrata, was found in the anteriorchamber of the right eye, attached loosely to the pupil's border by a fibrinous mass. Associatedconditions were iritis, subluxation of the lens, and secondary glaucoma. This is the firstdocumentation of human pentastomiasis in Israel.

Cases of human pentastomiasis involving the eye arerelatively rare. In so far as we have been able to tracethem, there are only 10 previous reports of ocularpentastomiasis: four of these are from the USA andwere due to larval Linguatula serrata'"4; the remain-ing six are from Africa and were caused by Armilliferarmillatus.5"The present case is of an Israeli Arab boy who

suffered from unilateral glaucoma secondary to iritiswhich was provoked by a larval Lingutulid. This is thefirst report of human pentastomiasis from Israel.

Case report

A 12-year-old Israeli Arab boy from a neighbouringvillage was referred to our clinic because of highintraocular pressure in his right eye. The boy said hehad suffered pain in his right eye for about a week,beginning after 'something believed to be a fly hit it'.On admission he had a visual acuity of 30 cm fingercounting on the affected right eye. The intraocularpressure was 48 mmHg by applanation. The corneawas oedematous, with some flare in the anteriorchamber. The pupil was 3 mm wide, round and free,the lens clear but with partial iridodonesis on thelower nasal quadrant. On ophthalmoscopy there wasa glaucomatous cupping of 0-8 cup/disc ratio in theoptic disc. Gonioscopy revealed several anteriorgoniosynechiae, particularly at 9 and 11 o'clock. Thevisual acuity of the left eye was 6/6, the intraocularCorrespondcncc to Yaron Lang MD. Department of Ophthal-mology, Ccntral Emek Hospital. Afula, Isracl.

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pressure was 12 mmHg, and the anterior andposterior segments were normal.

Secondary glaucoma of the right eye wasdiagnosed and the boy was given tablets of acetazola-mide 0-125 g four times a day, topical drops ofhomatropine 1% with topical steroids three times aday and timolol maleate 0-25% twice daily. Thefollowing day, on mydriasis, a subluxation of the lenswas observed. The intraocular pressure diminishedto 28 mmHg but increased again to 35-40 mmHg onsubsequent days. Nine days after admission, and onfailure of the conservative treatment, an uneventfultrabeculectomy was performed.On the first postoperative day, in the course of slit-

lamp examination, we noticed a white segmentedmass in the anterior chamber which was encased in afibrinous sheath and attached loosely to the pupil'sborder at 12 o'clock (Fig. 1). This fibrin coated andslightly crescent shaped mass changed its positionseveral times during the next few days. Laboratorytests, including a complete haematological examina-tion, gave normal results. Stool examinations forparasites were negative. Meanwhile there was noalleviation of the intraocular pressure.One week after the trabeculectomy the mass was

removed from the anterior chamber via limbalparacentesis. We were obliged to cut the fibrinoussheath in order to liberate the segmented mass and totake it out. After this procedure the eye became lessirritated, and in the next few days the intraocularpressure decreased markedly, to stabilise at 13-14mmHg.

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Fig. 1 Photograph (taken at a distance of35 cm) showingslightly crescent shapedforeign body loosely attached to theright eyepupil at 12 o'clock. This was diagnosed as a secondstage pentastomid larva, most likely ofLinguatula serrata.

Three weeks later the patient was dischargedhome. The visual acuity of the affected eye was then1/2 a meter finger counting and the intraocularpressure was 10 mmHg. The anterior segment wasnormal apart from the existence of fibrin remnants inthe anterior chamber, which were stretched over thelens and were attached to the limbal wound. Onophthalmoscopy the optic disc appeared pallid. Thefellow eye seemed to be the same as on admission.

After he was discharged the boy was lost to follow-up for almost a year. When he was traced andexamined at our outpatient clinic, there was nochange in the intraocular pressure of the right eye,and the visual acuity was about the same as ondischarge. However, a cataract had begun todevelop, and the optic disc seemed to have under-gone atrophy.

PARASITOLOGICAL FINDINGSThe extracted fibrinous mass had to be cut through inorder to release the object contained inside. Oncefreed, the latter could be examined under the dissect-ing microscope and later cleared in 10% KOH. Theobject measured 2 3 mm in length and 0-5 mm inmaximal width. It appeared to have undergone somedecomposition within its fibrinous sheath, and at first

Fig. 2 The pentastomid larva after removalfrom itsfibrousencasement. The specimen had undergone partialdecomposition, but body cavity and openings at both endswere still discernible. The body oflarva is only very sparselyannulated. x 9.

glance its cylindrical and slightly annulated shape wasreminiscent of a fly larva (Fig. 2). However, closerexamination after clearing failed to reveal thecharacteristic mouth hooks and posterior spiracles ofthe fly maggot, but instead showed the incipience ofthe anterior fang-like hooks typical of pentastomidinfective stages (Fig. 3). Under higher magnificationthe fine spination of the cuticle was revealed (Fig. 4),and this, together with the size measurements, theabsence of massive annulation of the body, and thegeographic location, finally led us to identify theobject as a secondary (second-stage) linguatulid larva(nymph), most likely of Linguatula serrata.

Discussion

The pentastomes or pentastomids are haemato-phagous metazoan endoparasites that as adults live inthe lungs of reptiles and birds or in the nasopharynxof mammals, usually carnivores. The larval-nymphal

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Intraocular pentastomiasis causing unilateral glaucoma

Fig. 3 Anteriorend ofpentastomid larva. Arrows markincipient hooks on the one side. Spination ofcuticlediscernible at anterior margin on right. x 18.

stages develop in a wide variety of vertebrate inter-mediate hosts, including man. Man, however, isusually an aberrant intermediate host, representing a

dead end for the parasite." The taxonomic positionof pentastomes is still obscure, and exact details ofthe life cycles of most of the species are little known.The pentastomes seem to occupy an intermediateposition between annelids and arthropods andhave been assigned to a separate phylum(Pentastomida" 12), but a more recent view'3 is that

tig. 4 further enlargement ofanterior extremity ofpentastomid larva revealing the spination (visible on rightside) exclusive to pentastomids ofgenus Linguatula. X 24.

they are a subclass within the Crustacea. Only sixspecies of pentastomes are known to infect man, andof these, two species, namely, Armillifer armillatusand Linguatulaserrata, account for more than 99% ofreported cases of human pentastomiasis. " Theformer is a species limited to Africa, while the latterhas been recorded from man in Africa, Europe(Germany, Switzerland, Italy, Greece, and Turkey),the Near East and Middle East, and the Americancontinent (Brazil, Chile, Colombia, Panama,Mexico, Cuba, and the USA)." 1'The present intraocular case was diagnosed as due

to a species of Linguatula and this for several reasons.Firstly, our patient has never travelled abroad. Thisrules out Armillifer armillatus and the related A.grandis, which are strictly African species. Secondly,the definitive hosts for Armillifer species are snakesof the genera Python and Bitis, 4 and neither of theseis represented in Israel. Thirdly, by its length (2.3mm) the pentastomid removed by us occupies anintermediary position between the length ascribed byHobmaier and Hobmaier'" for the second stage(0-35-0.5 mm) and third stage (4-6 mm) larva ofLinguatula rhinaria, now regarded as a synonym ofLinguatula serrata.'6 Finally, and most importantly,of third stage pentastome larvae (nymphs)encountered in man all have a smooth cuticle exceptthose of species of Linguatula, whose conspicuousipinules are sufficient to differentiate them from allthe rest." As Fig. 4 shows, our specimen bears therudiments of such spination, although it still lacks themassive body annulation and the crescent or cashewnut shape of the infective, third stage larva."As mentioned earlier, our patient has never travel-

led abroad, so clearly the infection was contractedlocally. Ours is the first report of human pentasto-miasis in Israel, and in view of the geographiclocation it is almost certain that we are dealing with alarval stage of the species Linguatula serrata. Theadult stages of this species reside in the nasopharynxof carnivores, mainly dogs and cats, and theseabound in Israel as well as in neighbouring Lebanon,where 44*3% of street dogs in Beirut have been foundto harbour L. serrata. 14

The life cycles of most species of pentastomes havenot been adequately studied, but that of L. serrata isfairly well known thanks, inter alia, to Hobmaier andHobmaier. 1' Briefly, the developmental cyclerequires carnivores (dogs and cats) as definitive hostsand herbivorous animals, mainly sheep and goats,as intermediate hosts. However, various othermammals, including man, can also serve as inter-mediate host. Eggs of the parasite, which are laid inthe upper air passages of the definitive host, arepassed to the exterior in its sputum or faeces, whencethey are ingested by the intermediate host with

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contaminated forage or water. The eggs hatch in theintestine, and the liberated first stage larvae, rarelyexceeding 250 Rum in length, penetrate the intestinalwall and migrate in the abdominal cavity to settle andultimately encyst in various organs but mainly in theliver and lymph nodes. After several moults withinthe cyst, the third stage larva (also called nymph orjuvenile) emerges from its cyst to migrate againthrough the peritoneal cavity before re-encysting invarious tissues and organs. When these are nowconsumed by the carnivorous definitive host, theinfective larva excysts to travel via the stomach andoesophagus to the nasopharynx, where, after severaladditional moults, it attains sexual maturity." 13 14Man-an aberrant intermediate host-usually

acquires the infection from egg contaminatedvegetables or water, or perhaps from intimate con-tact with an infected cat or dog," but also can becomeinfected by consuming the raw liver and/or lymphnodes of sheep and goats which contain the encystedtertiary linguatulid larvae. The latter form of humanpentastomiasis, characterised by severe naso-pharyngitis, is called the halzoun or marrarasyndrome,'7 and is prevalent in Lebanon, Turkey,and Greece."The present and similar cases of ocular pentasto-

miasis pose the interesting question as to how theparasite reaches this organ. The question hasintrigued several investigators' '8 and has yet to beresolved. In the present instance the patient claimedto have been hit in the eye by a fly a week prior to hisadmission. Some flies, such as Oestrus ovis, do infestthe human eye with their maggots, producingophthalmomyiasis, but there is no record as yet offlies serving as vectors of pentastomes, though therehas been one report of a cockroach (Periplanataamericana) serving as intermediate host for a lizardpentastome.'9 Moreover, the finding of a unilateralglaucomatous excavation of the optic disc and thepresence of several goniosynechiae in the boy's righteye strongly suggest a parasitic infection of a muchlonger duration than one week.From the life cycle of pentastomes, as briefly

described above, it is clear that both the first stagelarva (emerging from the egg) and the third stagelarva (after excystment) have a propensity for migra-tion in the body of the host. Might not the micro-scopic first stage larva, which rarely exceeds 250 umin length, inadvertently enter a blood vessel, in thecourse of its penetration through the intestinal wall,and be transported to the eye? We believe this is atleast theoretically feasible, and other parasites, suchas Entamoeba histolytica, do occasionally travel inthe blood stream to reach the human brain. Since themigratory pentastome stages are endowed with pro-teolytic capabilities, these could explain the observed

zonulolysis and subluxation of the lens in the presentcase. Alternatively, in the cases of halzoun syn-drome, might not the liberated third stage larvaaccidentally travel from the nasopharynx to the eyevia the nasolacrimal duct, which is a sufficiently wide,non-ciliated passageway? We believe this to be anequally feasible explanation for some cases of ocularinvolvement due to Linguatula serrata, but in ourcase the first conjecture is preferable because therecovered parasite was apparently a second stagelarva and there was no history of halzoun. Theinfection could readily have been acquired from eggcontaminated vegetation or water, because the boylived under very poor sanitary conditions and admit-ted drinking water from doubtful sources.Localisation of pentastomid larvae in the anterior

chamber is apparently rare, for only a few cases havebeen reported.'I3 Ocular manifestations of penta-stomiasis are equally rare, and indeed Fain'6 refers toocular infections as being free of lesions. Our case,however, did involve unilateral glaucoma secondaryto iritis and in this respect and also in its aetiology, isalmost identical to that reported by Deweese et al.-from a Negro girl.

References

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