EXTERNAL OPHTHALMOMYIASIS: A CASE REPORT

VERSTRYNGE K.*, FOETS B.*

SUMMARY sis. De patiënt meldt zich met symptomen van een virale conjunctivitis, zoals tranen, jeuk, hyperemie Many dipteran can cause ophthalmomyiasis, a en vreemd-voorwerpgevoel. De aandoening is zelfli- potentially severe and vision threatening disease. We miterend en verwijdering van de larven is de meest report a case of ophthalomyiasis caused by efficiënte behandeling. Identificatie van het speci- ovis. Larvae of Oestrus ovis are confined to the sur- men is belangrijk om gevaar voor penetratie in de face of the eye and cause external ophthalmomyia- oogbol in te schatten. sis. The presentation is similar to a viral conjunc- tivitis, with tearing, itching, hyperaemia and foreign KEY WORDS body sensation. The disease is self-limiting and re- moval of the larvae is the most effective therapy. External ophthalmomyiasis, Oestrus ovis Identification of the species is important to estimate the risk of penetration of the globe. MOTS-CLÉS RÉSUMÉ Ophtalmomyiase externe, Oestrus ovis De nombreuses mouches diptères peuvent causer l’ophtalmomyiase, qui peut être sévère et menaçan- te pour la vue. Nous rapportons un cas d’ophtalmo- myiase causé par l’Oestrus ovis. Les larves d’Oes- trus ovis sont circonscrites à la surface oculaire et provoquent l’ophtalmomyiase externe. La présenta- tion est similaire à une conjonctivite virale, avec lar- moiement, démangeaison, hyperémie et sensation de corps étranger. La maladie est circonscrite et l’en- lèvement des larves est la thérapie la plus efficace. L’identification de l’espèce est importante pour es- timer le danger de pénétration dans le globe. SAMENVATTING Vele diptere vliegen kunnen oftalmomyiasis, een po- tentieel ernstige en visusbedreigende aandoening, veroorzaken. Wij beschrijven een geval van oftal- momyiasis veroorzaakt door de vlieg Oestrus ovis. De larven van de Oestrus ovis blijven gelimiteerd tot het oogoppervlak en leiden tot externe oftalmomyia-

zzzzzz * University Hospitals Leuven, Department of Ophthalmology.

received: 21.09.04 accepted: 08.11.04

Bull. Soc. belge Ophtalmol., 294, 67-71, 2004. 67 INTRODUCTION swab, with one maggot causing a small con- junctival bleeding on attempt of removal. Their is the infestation of live human and ver- mobility did not slow after instillation of oxy- tebrate with dipterous larvae, which, buprocaine. After photographic documentation, at least for a certain period, feed on the host’s we removed the maggots with a forceps. A con- dead or living tissue, liquid body-substances or junctival sac washout with saline solution was ingested food (11) and subsequently may cause performed. In order to kill possibly remaining different clinical pictures. Oestrus ovis ( maggots by dehydration, hypertonic saline oint- nasal ) is one of the most common caus- ment was administered. The otorhinolaringol- es of human myiasis. The normal hosts for the ogist performed an endoscopy of the nose and larvae are sheep and . Occasionally, hu- sinuses, because the patient also complained mans are the intermediate hosts, with the eye of watery nasal discharge. This examination re- as the site of infestation. The clinical picture is vealed a congested nasal mucosa. On follow- that of a viral or allergic conjunctivitis with tear- up examination two days later, no residual mag- ing, foreign body sensation and itching of the gots could be found and the patient was free of eye. This is the first report of an imported case symptoms. of external ophthalmomyiasis in Belgium. The maggots were identified as larvae by means of the slitlamp pictures by the Depart- CASE REPORT ment of Microbiology of the University of Leu- ven and by the Institute of Tropical Medicine A 26-year-old woman was referred to the Ca- of Antwerp. They were segmented and had two sualty Department of the University Hospitals large dark oral hooks, connected to a white in Leuven with foreign body sensation, irrita- cephalopharyngeal skeleton. The body was trans- tion and tearing of the right eye. The symp- lucent (fig 1b). A more definitive identification toms began 24 hours earlier, on returning from was not possible because the larvae were dead a holiday to Crete. She did not remember be- and had not been properly preserved. ing struck in the eye or face by any . Her ophthalmologic history was negative. DISCUSSION On examination we found a slightly congested conjunctiva, but otherwise quiet anterior seg- Ophthalmomyiasis is classified as orbital, ex- ment with five small (1mm), transparent, mov- ternal or internal, based on the site of larval in- ing maggots in the fornix, on the plica interna vasion. Large numbers of larvae invading and and under the upper eyelid (fig 1a). The mag- destroying orbital contents cause orbital myia- gots avoided the slitlamp beam, as they were sis. External ophthalmomyiasis refers to super- photophobic. They stuck to the conjunctiva and ficial infestation of ocular tissue, including the were very difficult to remove using a cotton conjunctiva. Internal ophthalmomyiasis occurs

Fig. 1a: maggot on the conjunctiva near the plica interna Fig. 1b: maggot with translucent and segmented body and two large dark oral books connected to a white cephalo- pharyngeal skeleton

68 Fig. 2: Oestrus ovis: adult Fig. 3: life cycle of Oestrus ovis when the larvae penetrate the sclera and bur- milky fluid onto the nostrils of the host. Direct row in the subretinal space. contact between the fly and its host is not ne- Three dipteran families are considered as the cessary for the infestation (7). The larvae of main causes of myiasis in humans. These fami- Oestrus ovis mature in the mucus membrane lies include Oestridae, Calliphoridae and Sar- of the nasal cavities. Ultimately, they are sneezed cophagidae (9). External ophthalmomyiasis is onto the soil where they pupate to become an often a benign self-limiting disease (1, 2, 3, 7, imago (fig 3). The Oestrus ovis larvae have no 8, 14, 17, 18), in contrast with internal oph- bite organisms and are unable to secrete pro- thalmomyiasis which can lead to severe loss of teolytic enzymes, so that they are mostly con- vision or even loss of the eye. If the infestation fined to the outer membranes of the eye (3). is caused by larvae with burrowing habits, they However, small conjunctival hemorrhages may can give rise to very destructive forms of oph- be apparent at sites where the larva clings with thalmomyiasis, especially in debilitated pa- its mouth claws. In man the larvae cannot sur- tients (3, 4, 6, 10, 16, 19). Fly species of the vive beyond the first larval stage and are be- genera Calliphora, Lucilia, Sarcophaga, Gas- lieved to die within ten days if not removed terophilus, Hypoderma (5), Musca, Callitroga, (11). In the human conjunctiva they can cause Cuterebra (4, 12, 13), Dermatobia, Chrysomy- a great deal of irritation, lacrimation, pain and ia, Wohlfahrtia and Oedemagena (6) are known inflammation, which should be differentiated to cause internal ophthalmomyiasis in humans. from an allergic reaction or viral conjunctivitis. Oestrus ovis (sheep nasal botfly) (class: Insec- As the larvae are small, translucent and quick- ta, order: Diptera and family: Oestridae) is the ly avoiding the slitlamp beam, they can be eas- most common cause of human myiasis (14). ily overlooked. Grammer et al. summarized nu- The adult insect is slightly smaller than a hon- merous cases of external ophthalmomyiasis due eybee (fig 2). Its mouthparts are vestigial. The to Oestrus ovis (7). fly is ubiquitous, but most common in shep- Exact taxonomic classification of dipterous lar- herding areas. The normal hosts of the larvae vae that have been removed from superficial include sheep and goats. Occasionally, due to parts of the eye is important for estimating the an aberration in the life cycle (7), man is the potential risk of intraocular penetration of pos- intermediate host of which the eye is the site sibly remaining larvae not found during slit- of infestation. Poor health of sheep and farm- lamp examination. Removed larvae should be er, close contact between animals and man, preserved in 70% alcohol and sent to special- and generally poor living conditions may be ists for examination. Especially the caudal por- contributing factors to the likelihood of human tion (posterior spiracles) and the cephalopha- infestation. The gravid adult female fly swarms ryngeal skeleton of the larva are important for around the head of the animals and ejects the exact identification (11). However, in emergen- first-instar larvae, which have previously hatched cy situations it is not always easy to estimate from the eggs in the fly vagina, in a stream of the probable danger of a rare disease and know-

69 ledge of microbiologic preserving and cultur- (3) DE VRIES L.A.M., VAN BIJSTERVELD O.P. − ing techniques is not evident. Our experience Ophthalmooestriasis conjunctivae. Ophthal- showed that larvae quickly die and dry out once mologica 1986; 192: 193-197. − removed from the eye. We could not immedi- (4) DIXON J.M., WINKLER C.H., NELSON J.H. ately find specialists to help us preserving the Ophthalmomyiasis interna caused by Cutere- bra larva. Am J Ophthalmol 1971; 1: 415- species in a good way. We therefore tempted 416. to identify the larva as Oestrus ovis based only (5) EDWARDS K.M., MEREDITH T.A., HAGLER on biomicroscopic appearance (translucent body, W.S., HEALY G.R. − Ophthalmomyiasis inter- segmentation, large dark oral hooks connect- na causing visual loss. Am J Ophthalmol 1984; ed to a white cephalopharyngeal skeleton) and 97: 605-610. extended study of the literature. Arguments (6) GJOTTERBERG M., INGEMANSSON S.O. − In- strongly in favour of infestation with larvae of traocular infestation by the reindeer warble fly Oestrus ovis are the region of infestation, the larva: an unusual indication for acute vitrec- season, clinical manifestation and microscop- tomy. Br J Ophthalmol 1988; 72: 420-423. ic characteristics of the larvae. (7) GRAMMER J., ERB C., KAMIN G., WILD M., RIEDINGER C., KOSMIDIS P., PLEYER U., Except for mechanical removal, there is no oth- THIEL H. − Ophthalmomyiasis externa due to er therapy described. In contrast to our expe- the sheep botfly Oestrus ovis (Diptera: Oestri- rience, topical anaesthetics are said to para- dae) in southwest Germany. Germ J Ophthal- lyse the larvae (15). Topical steroids relieve mol 1995; 4: 188-195. symptoms. Topical antibiotics are useful in pre- (8) GROH M.J.M., JUNEMANN A., ZILCH R. − venting secondary infection by bacteria. Follow- Ophthalmomyiasis externa durch Oestrus ovis up examination by an ophthalmologist is re- in Franken. Klin Monatsbl Augenheilkd 1998; commended to avoid the possible complica- 213: 60-62. − tion of internal ophthalmomyiasis. (9) HAKIMI R., YAZDI I. Oral mucosa myiasis caused by Oestrus Ovis. Arch Iranian Med 2002; 5: 194-196. (10) JAKOBS E.M., ADELBERG D.A., LEWIS J.M., CONCLUSION TRPIS M., GREEN R. − Ophthalmomyiasis in- terna posterior. Retina 1997; 17: 310-314. This is by our knowledge the first report of an (11) LANE R.P., CROSSKEY R.W. − Medical insects imported case of external ophthalmomyiasis by and arachnids. London: Chapman & Hall. Text- Oestrus ovis in Belgium. We describe a typical book: 1993; 429-469. case of external ophthalmomyiasis most likely (12) NEWMAN P.E.,BEAVER P.C.,KOZARSKY P.E., due to Oestrus Ovis. Although external ophthal- WARING G.O. − Fly larva adherent to corneal momyiasis is an uncommon condition in north- endothelium. Am J Ophthalmol 1986; 102: ern Europe, one should be cautious for import- 211-216. ed cases in travellers from Mediterranean ar- (13) PERRY H.D., DONNENFELD E.D., FONT R.L. − Intracorneal ophthalmomyiasis. Am J Oph- eas or elsewhere. Some fly species are capa- thalmol 1990; 190: 741-742. ble of penetrating the globe, causing internal (14) REINGOLD W.J., ROBIN J.B., LEIPA D., KON- ophthalmomyiasis, which is sight-threatening. DRA L., SCHANZLIN D.J., SMITH R.E. − Oes- Therefore, taxonomic differentiation is impor- trus ovis ophthalmomyiasis externa. Am J Oph- tant. thalmol 1984; 97: 7-10. (15) SIGAUKE E., BEEBE W.E., GANDER R.M., CA- VUOTI D., SOUTHERN P. − Case report: Oph- REFERENCES thalmomyiasis externa in Dallas county, Texas. Am J Trop Med Hyg 2003; 68: 46-47. (1) CAMERON J.A., SHOUKREY N.M., AL-GAR- (16) SIVARAMASUBRAMANYAM P., SADANAND NI A.A. − Conjunctival Ophthalmomyiasis cau- A.V. − Ophthalmomyiasis. Br J Ophthalmol sed by the sheep nasal botfly (oestrus ovis). 1968; 52: 64-65. Am J Ophthalmol 1991; 112: 331-334. (17) STEVENS J.D., McCARTNEY A.C., HOWES R. (2) CHODOSH J., CLARRIDGE J.E., MATOBA A. − Oestrus ovis ophthalmomyiasis acquired in − Nosocomial conjunctival ophthalmomyiasis the UK: case report and scanning electron mi- with Cochliomyia macellaria. Am J Ophthal- croscopic study. Br J Ophthalmol 1991; 75: mol 1991; 111: 520-521. 702-703.

70 (18) WONG D. − External ophthalmomyiasis cau- We would like to thank Prof. De Loof of the De- sed by the sheep bot Oestrus ovis L. Br J Oph- partment of Physiology and Neurobio- thalmol 1982; 66: 786-787. logy of the University of Leuven and Dr. Wim (19) ZIEMIANSKI M.C., LEE K.Y., SABATES F.N. − Van Bortel of the Institute of Tropical Medicine Ophthalmomyiasis Interna. Arch Ophthalmol in Antwerp for helping us identifying the larvae. 1980; 98: 1588-1589. zzzzzz Correspondence: Dr. K.Verstrynge, University Hospitals Leuven, Department of Ophthalmology, Kapucijnenvoer 33, 3000 Leuven, Belgium. E-mail: [email protected]

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