Ophthalmomyiasis externa caused by Oestrus ovis

Abstract

This report describes the case of a woman in her early 20s who presented with a 3-day history of mobile foreign bodies and watering from her right eye. She had recently returned from vacation on a Greek island and presented to an ophthalmology unit in London, UK. A sample taken demonstrated Oestrus ovis infestation and confirmed the diagnosis of ophthalmomyiasis externa. She was treated with prophylactic topical antibiotics and subsequently made a full recovery. This was only the sixth presentation of O. ovis ophthalmomyiasis externa documented within the UK and the only case documented within the last 20 years. This is the fifth documented case found to have been transmitted within Greece.

Background

Ophthalmomyiasis externa refers to the superficial infestation of the ocular structures by dipterous larvae. It is considerably more common than ophthalmomyiasis interna—an intraorbital infestation; however, it remains an exceptionally rare clinical entity especially within the UK. Only six prior cases have been described in the UK since 1951. The most common organism causing ophthalmomyiasis externa is the obligate parasite Oestrus ovis (commonly known as ‘sheep bot fly’) although other species of Diptera have been associated, including Rhinoestrus purpureus, Dermatobia hominis and Chrysomya bezziana.¹ Typically, an adult female O. ovis deposits first instar larvae within the nostrils of small ruminants in an act termed larviposition. These larvae migrate and mature within the paranasal sinuses, developing into third instar larva, before subsequent expulsion from the nasal passages over the course of weeks or months.² Humans are accidental hosts, and there is no evidence that the first instar larvae fully mature within the human host.¹ Due to the close association with small ruminants, case reports tend to locate infections within rural communities that remain in close contact with animal and are largely within the Mediterranean region, the Middle East, South Asia and New Zealand.³ There are only five previous cases of O. ovis ophthalmomyiasis externa reported from within Greece. We report a rare case of O. ovis ophthalmomyiasis externa, presenting within a London eye unit.

Case presentation

A student in her early 20s with no relevant comorbidities attended the eye casualty department of a London teaching hospital in late summer 2020. She presented with a 3-day history of conjunctival injection, foreign body sensation and epiphora in the right eye and reported seeing mobile foreign bodies on the surface of the right eye. She had returned from vacation on a Greek island, 2 weeks earlier, and denied any contact with animals during this visit. Clinical examination demonstrated two mobile transparent organisms around 1 mm in length with anterior black jaw structures, segmentations and a longitudinal spine (video 1). One organism was situated within the lower tarsal conjunctiva and another superficially within the subepithelial cornea. These demonstrated no phototaxia. There was superficial fluorescein staining of the corneal epithelium in a tracking pattern with no stromal invasion or inflammation (figure 1). Despite the corneal epithelial changes, visual acuity remained unaffected. The intraocular examination was unremarkable with no evidence of ophthalmomyiasis interna.

Video 1. The mobile Oestrus ovis larva can be seen on the inferior tarsal conjunctiva. Anterior dark structures are evident.

bcr-2022-249796supp001.mp4 ^{(668.9KB, mp4)}

DOI: 10.1136/bcr-2022-249796.video01

Figure 1.

(A) Corneal fluoresceine staining pattern demonstrating disruption of the corneal epithelium. (B) Oestrus ovis larva evident on lower tarsal conjunctiva.

Investigations

Following instillation of topical anaesthetic, parasite removal with a cotton bud was performed, and the samples were collected in sterile water and transported to the local microbiology laboratory. Light microscopy identified the parasites as larvae of O. ovis. The identification was confirmed by the London School of Hygiene and Tropical Medicine Diagnostic Parasitology Laboratory as first instar O. ovis larva. The mouthhooks and cephalopharyngeal skeleton are the key to the identification (figure 2).

Figure 2.

Anterior region of the Oestrus ovis larva demonstrating classical mouthhooks and cephalopharyngeal skeleton of first instar O. ovis on microscopy. HPS, hypopharyngeal sclerite; MH, mouthhooks; PS, pharyngeal sclerite.

Differential diagnosis

The presentation of lacrimation, hyperaemia and foreign body sensation has a broad differential diagnosis including viral, bacterial and allergic conjunctivitis. Additionally, the corneal staining pattern arouses suspicion of corneal abrasion or a subtarsal foreign body. The diagnosis was evident in this case following the direct visualisation of the O. ovis larvae.

Treatment

Following removal of the larvae, the eye was irrigated with 1 L of NaCl 0.9% fluid. Chloramphenicol 1% ointment four times per day for 1 week to the affected eye was prescribed, and the patient was advised to report any further symptoms.

Outcome and follow-up

On return 1 week later, symptoms and examination abnormalities had entirely resolved. There was no evidence of additional larva or egg hatching, and the corneal surface had healed without scarring. Her vision remained excellent in both eyes. She did not attend further review due to prior educational commitments.

Discussion

O. ovis ophthalmomyiasis typically presents with acute unilateral foreign body sensation, conjunctival injection, lacrimation, itching and pain.³ Examination may demonstrate a mobile foreign body, conjunctival haemorrhages, pseudomembrane formation and superficial punctate keratopathy.¹ Cases of O. ovis ophthalmomyiasis externa have been shown to rarely cause stromal keratitis and anterior uveitis.⁴

Treatment is based on anecdotal evidence with poor consensus on the optimal regime. Veterinary medicine experience sets a precedent for the use of Ivermectin; however, evidence for this in human ophthalmomyiasis externa is lacking.¹ As a single dose of Ivermectin would aid concurrent treatment of nasal myiasis and has generally mild, transient side effects, off-label use of Ivermectin is worth considering.⁵ It is generally accepted that mechanical removal under topical anaesthesia followed by prophylactic topical antibiotics is sufficient to achieve cure of purely external ophthalmomyiasis.^{1 5}

To date, there have been only five documented cases of O. ovis ophthalmomyiasis externa contracted within Greece. Keller et al describe the first case, occurring in a young boy returning from vacation in 1991.⁶ Talks and Wölfelschneider and Wiedemann describe two cases where O. ovis infestation occurred following a vacation to Rhodes.^{7 8} Fries et al describe a case in a travelling climber on another Greek island who had extensive contact with sheep,⁹ while Hartmannová et al describe a case contracted in northern, mainland Greece.¹⁰ Other than the case described by Fries et al, there were no reports of extended animal contact. In terms of patient presentation within the UK, Smith, Romanes and Stevens et al each described a single case with infection occurring within mainland UK,^11–13 while Wong, Talks and Bainbridge and Rostron report the only three cases of imported disease in the UK evident within the literature.^{7 14 15} There have been no cases described in the UK in the last 20 years.

The Mediterranean distribution of O. ovis ophthalmomyiasis externa was described in a systematic review by Pupić-Bakrač et al.³ This review included 259 cases of O. ovis ophthalmomyiasis externa within Mediterranean countries since 1954, with the majority of infection within Libya (n=121), Tunisia (n=38), Turkey (n=29), Italy (n=28), France (n=15) and Spain (n=15).³ Further cases in tourists travelling to Italy have subsequently been described.¹⁶ Data describing the global prevalence and incidence of O. ovis ophthalmomyiasis externa is lacking. Case reports describe infrequent infections within the Middle East,^17–19 North America,²⁰ South Asia,^{21 22} New Zealand⁵ and Hawaii;²³ however, global infection rates are likely to be under-reported.

Although humans most at risk of O. ovis ophthalmomyiasis externa were traditionally thought to be typically those in close contact with animals, specifically farmers and shepherds, an analysis of the above systematic review identified these to be relatively weak risk factors. Risk factors discussed included rural residence (vs urban—HR 1.36), animal contact (vs no reported contact—HR 1.31) and fly contact (vs no reported contact—HR 1.62).³ The quality of this data is limited due to its retrospective nature and reporting bias.

A recent meta-analysis of O. ovis infestation in sheep and goat populations demonstrated that European ruminant populations had the highest disease burden (57%), while North and South America populations had the lowest prevalence (34%) mirroring the trends within human disease.²⁴ Optimal temperature for larviposition is 25°C–28°C, and temperatures below 12°C or above 38°C lead Oestrus to remain dormant and impairs development, respectively.²⁵ Climate change and increased air temperature may affect O. ovis populations leading to increased transmission both within the ruminants and zoonotic infection within humans.

This case highlights the importance of both a thorough travel history and a high level of suspicion in cases of returning travellers from endemic regions with the clinical presentation reported. The linear epithelial abrasions within the cornea could be mistaken for a subtarsal foreign body with superficial epithelial abrasions and highlight the importance of thorough examination of the fornices including lid eversion.

Patient’s perspective.

When I first started feeling irritation in my eye, I initially dismissed it as some dirt or an eyelash, but as the irritation got worse and my eyelid started to swell and close slightly, I knew that something wasn't right. I was horrified when I started feeling and seeing movement from the larvae in my eye, as it’s not something I'd heard of before. After visiting the hospital team, I was put at ease and reassured, despite this being almost unheard of. I'm still unsure how the botfly larvae ended up in my eye, but I'm glad that I trusted my instincts and sought medical help when I did. I'm incredibly grateful to the team for their support and prompt diagnosis!

Learning points.

• Although this condition is rare, it illustrates the importance of enquiring regarding the travel history in cases of atypical epithelial corneal staining.

• Ophthalmomyiasis externa may present in locations remote to transmission sites even following brief periods of travel.

• Disease may occur in otherwise young, healthy individuals with no ocular surface disease or reported animal contact.

Ethics statements

Patient consent for publication

Consent obtained directly from patient(s).