Optometry & Vision Science:
Ophthalmomyiasis Caused by the Sheep Bot Fly Oestrus ovis in Northern Iraq
GREGORY, ANDREW R. OD, FAAO; SCHATZ, SCOTT OD, PhD, FAAO; LAUBACH, HAROLD PhD
U.S. Army 101st Airborne Division (ARG), Colleges of Optometry (SS), and Medical Sciences (HL), Nova Southeastern University, Fort Lauderdale, Florida
Funding was provided by an intramural grant from Nova Southeastern University.
Submitted December 17, 2003; accepted March 23, 2004.
Myiasis is the feeding of fly larvae on vertebrates. The sheep bot fly larva of Oestrus ovis is a mammalian parasite of the skin, nose, ears, and eyes. When the larvae infest and feed on the structures of the eye, the condition is termed ophthalmomyiasis. Most often this infestation is limited to the external structures of the eye and is referred to as ophthalmomyiasis externa. The features of this condition are severe local inflammation, positive foreign body sensation, erythema, and lacrimation. Vision may or may not be reduced, depending on involvement of the cornea. A 20-year-old white male soldier sought treatment for an inflamed eye and an irritated cornea OS. His eyelids were swollen with marked periorbital edema and conjunctival erythema OS. On slitlamp examination, small whitish organisms were viewed on the conjunctiva OS. The organisms were removed, preserved, and sent to Nova Southeastern University where they were identified as O. ovis first-stage larvae. The patient was treated with antibiotic ointment, and the inflammation resolved within 1 week. O. ovis has a worldwide distribution, and although sheep are the preferred host, humans may also serve as an intermediate host in the organism’s life cycle. This case represents one of several reports of ophthalmomyiasis in the Middle East caused by O. ovis. U.S. troops stationed in Iraq and surrounding areas are vulnerable to eye infestation by fly larvae, and health care providers need to include this condition in their differential diagnosis of anterior segment inflammatory disorders.
Myiasis is a parasitic disease caused by dipteran fly larvae of several species, including the sheep bot fly Oestrus ovis. The preferred intermediate host is typically sheep and goats, but occasionally this organism infests humans. The first-stage larvae are obligate parasites that burrow their way into host tissues.1 The host disease state is referred to as ophthalmomyiasis when the larvae are found on and within ocular tissues.
The sheep bot fly O. ovis is found throughout much of the world. Adult female flies are larviparous: the eggs hatch while still inside the female fly, and she deposits the larvae onto mammalian hosts while still in flight.2,3 Hennessy et al.4 report that infection can also occur by direct contact of a female fly with host mucous membranes or by the inadvertent transfer of larvae via infested water splashing onto the host’s face and eyes. The primary site of a myiasis infestation is usually the nose, ears, eyes, and surrounding skin of the host but can also include the pharynx and the gastrointestinal and genitourinary tracts.2,5 Occasionally the female bot fly will deposit the larvae on a human host rather than a sheep or a goat. This tends to occur in areas where sheep are raised near humans. Zumpt6 postulated that humans are most commonly infested in geographic regions where the population density of sheep and goats is low relative to the human population.
Myiasis caused by O. ovis infestation has been reported to have a broad pantropical, subtropical/temperate distribution that includes parts of Europe,7–10 North America,11–13 New Zealand,14 and Australia.15,16 However, the majority of the cases reported in the literature come from the arid region extending from North Africa through the Middle East to southern Asia,2,6,17–29 including three reports from Iraq.30–32
Herein, a case of ophthalmomyiasis caused by O. ovis that occurred on an American soldier in northern Iraq is reported.
Hospital staff referred a 20-year-old white male soldier to the optometry clinic in Mosul, Iraq. He unsuccessfully had his left eye irrigated by unit medics and the hospital staff for a corneal foreign body, reported to be wooden in nature, which had been present for 2 days. He complained of lacrimation and photophobia OS. Uncorrected distance visual acuity measured 20/15 in each eye. Extraocular motilities were full, extensive, smooth, and accurate. Confrontation fields were full to finger counting in both eyes, and pupils were equal, round, and reactive to light and accommodation with no afferent pupillary defect in either eye. The patient had periorbital edema and erythema OS, and the eyelids were slightly warm when touched. The conjunctiva showed grade 3 injection with mild chemosis. Sodium fluorescein staining revealed a corneal foreign body located off of the visual axis at the 4-o’clock position OS. Anterior chamber was deep and quiet in both eyes. The foreign body was removed with a spud after instillation of tetracaine. Lid eversion revealed no other foreign bodies.
The assessment at this visit was preseptal cellulitis secondary to a corneal foreign body OS. The patient was prescribed ciprofloxacin hydrochloride every 2 h while awake with erythromycin ointment to be instilled every night. Oral azithromycin was prescribed in the form of a Z-pack. Tramadol hydrochloride, 50 mg, was prescribed for pain. The patient was instructed to return for follow-up evaluation the next day.
The patient returned as instructed the following day and reported significant improvement in pain and light sensitivity but also reported that he had misplaced the bottle of ciprofloxacin hydrochloride that morning. The periorbital edema and erythema remained unchanged. Uncorrected visual acuity remained 20/15 in each eye. Examination with sodium fluorescein stain revealed complete reepithelialization of the corneal defect. The lids were again everted to ensure no foreign bodies were missed the previous evening. A nonstaining white area, similar in appearance to mucus, was observed on the superior palpebral conjunctiva. This was removed with a cotton-tipped applicator (Fig. 1). At the moment of removal of the object, it appeared to move. The swab was then studied under high magnification via the slitlamp and revealed that the foreign body was actually a live organism that had a clear, segmented body with brown “pinchers” and internal organs (Fig. 2). Photographs were taken of the organism through the slitlamp. A more detailed examination of the eye under high magnification revealed the presence of three additional organisms located in the medial and lateral canthus areas. These were photographed (Fig. 1) and then removed using jewelers forceps. One specimen was retained for analysis and identification. The entomologist assigned to northern Iraq was consulted, and a tentative identification of the organisms was larvae of the sheep bot fly O. ovis. The preserved sample was shipped to Nova Southeastern University, Colleges of Optometry and Medical Sciences in the United States, where positive identification of O. ovis was made and photodocumented.
The patient was instructed to complete a regimen of oral azithromycin as prescribed the previous evening and to increase the frequency of the erythromycin ointment to every hour. The next day, when the patient returned for follow-up evaluation, there was significant improvement in the periorbital edema and erythema. Visual acuity was unchanged. A dilated fundus examination was performed at this visit, revealing healthy internal ocular structures. The patient continued to show improvement with complete resolution within 1 week.
The reported Middle Eastern cases of myiasis are from the Baghdad area of Iraq, southern Iran, Kuwait, Oman, Saudi Arabia, Jordan, Israel, and Egypt. All the reported cases from this region seem to have occurred between April and September. The case reported here accounts for the northernmost report of myiasis caused by O. ovis in the Middle East region and is also the case that occurred latest in the calendar year, a time that coincides with population peaks of sheep bot flies.31
The occurrence of the sheep bot fly in Iraq was reported by Al-Dabagh et al.,30 Abul-Hab,31 and Helmi et al.32 In a study on the seasonality of sheep bot fly infestations on sheep and goats in central Iraq, Abul-Hab found a high level of infestation occurred from September to January.31 No larvae were observed from February to June. Hira et al.23 reported spring and autumn bimodal peaks in occurrence. By contrast, Knapp and Rogers33 found activity throughout the year on sheep in Kentucky. Reingold et al.12 did not mention a seasonal predilection in their report on 16 cases of sheep bot fly ophthalmomyiasis in Santa Catalina Island off the California coast. Other reports of cases of O. ovis ophthalmomyiasis externa in the United States were reported by Sigauke et al.13 (Texas), Heyde et al.34 (California), Rao et al.35 (Georgia), Bosniak and Schiller36 (New York), and Meleney et al.37 (southwestern United States).
When dipteran larvae infect a human, the disease is referred to as human myiasis. When the eye is involved, the disease is called ophthalmomyiasis, and distinction may be made as to whether the parasite is located in external or internal ocular tissues.38,39 External ophthalmomyiasis is typified by mild to acute conjunctivitis, pseudoorbital cellulitis, and superficial punctate keratitis.9,12,38 Engelbrecht et al.40 reported on the occurrence of a preseptal cellulitis secondary to Cuterebra sp. larval infection of a patient in North Carolina. If the larvae penetrate the globe, the host may have a poor visual outcome.25,41 In addition to O. ovis other dipteran larvae that have been reported to be the etiologic agents of ophthalmomyiasis include Hypoderma bovis, Hypoderma lineatum, Edemagena tarandi, Cuterebra sp., Gastrophilus intestinalis, Cochliomyia macellaria, and Rhinoestrus purpureus.42,43 Although O. ovis is the most common etiologic agent of ophthalmomyiasis on a global basis, Goodman et al.44 report that the human bot fly Dermatobia hominis is the most common cause of cutaneous myiasis in Central and South America. The disease ranges from being seasonal in dry arid environments to continuous throughout the year in more humid temperate areas.41
Giannetto et al.45 presented a scanning electron micrograph study of O. ovis in Sicily. They described the structural adaptation of O. ovis, including the hooks and cat’s claw-shaped spines used by the organism to attach onto the host and penetrate the host tissues. The parasite gains its nutrition by ingesting the inflammatory exudate of the host that is induced by the parasite’s activities.45 If the parasite is restricted to the ocular surface, it will not live beyond the first larval stage, and the inflammation is short-lived. However, if the parasite is able to penetrate into the interior of the eye, a more severe inflammation will develop.39,45,46 Infestations of the posterior segment by Cuterebra sp. may result in subretinal hemorrhages, linear retinal streaks or tracks, and moderate to severe posterior uveitis and may require vitrectomy for surgical removal of the larvae.40,47,48
Untreated cases of ophthalmomyiasis externa do not always produce serious eye damage unless secondary bacterial complications ensue. Therefore, unidentified, untreated cases can resolve and go unreported. The authors believe that only a small proportion of actual human eye infestations are reported and that the few reports in the literature are reflective of the lack of definitive diagnosis of ophthalmomyiasis caused by larva of O. ovis or other species of flies.
Management of superficial infections includes antibiotic therapy and corticosteroids to alleviate the inflammatory response. It is advisable to use a topical anesthetic when removing the larvae from the ocular surface not only for the benefit of the patient but also to loosen the larval attachment to the ocular surface. Because the larvae migrate along the mucous tissue of the conjunctiva, it is necessary to double evert the eyelids to ensure that all the larvae have been removed. The inflammatory state of the conjunctiva is usually resolved within a few days, but if signs and symptoms persist for more than 1 week, a deeper penetration into the ocular tissues needs to be considered.
Myiasis is generally considered an occupational risk of raising sheep or goats. In this case, the intermediate human host was an American soldier serving at a post in Mosul, Iraq near the Tigris River. There were many sheep in the general area, but none were inside the military compound. With the increased frequency and length of deployments of our military around the world, it is important for all health care providers, military and civilian alike, to be aware of the increased risk of exposure to a wide variety of conditions, such as ophthalmomyiasis, that may otherwise not be on the providers’ list of differential diagnoses.
We thank the U.S. 101st Airborne Division for its cooperation.
College of Optometry
Nova Southeastern University
3200 South University Drive
Fort Lauderdale, FL 33328
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