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Ophthalmomyiasis
Introduction
Maggot infestations of humans are not uncommon. Ocular surface infestation is a well-known fact and has been reported from different parts of the world.[1][2][3] The word "myiasis" has been derived from the Greek word "myia," which means fly.[4][5] Ophthalmomyiasis refers to the infestation of the eye by the larvae. If the infestation is confined to the ocular surface or periorbital tissues, it is termed as ophthalmomyiasis externa; whereas, intraocular penetration of larva is referred to as ophthalmomyiasis interna.[5][6]
The disease is often underreported and adds to morbidity. Considering the rarity of the disease, the presentation of the disease needs to be known to have a strong suspicion. It was considered to be associated with poor hygiene.[7] However, subsequent studies revealed that ophthalmomyiasis could be unrelated to hygiene.[8] This article highlights the etiology, geographical distribution, clinical features, diagnostic challenges, and potential complications of ophthalmomyiasis.
Etiology
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Etiology
The type of ophthalmomyiasis depends on the nature of larvae. Facultative parasites require dead necrotic tissues, whereas obligate parasites require vital living tissues and tend to penetrate intraocularly.[9] The various larval forms of different flies causing ophthalmomyiasis are:
1. Oestrus ovis (sheep botfly)[10]
2. Phaenicia lucilia[11]
3. Dermatobia hominis[12]
4. Musca domestica[5]
5. Hypoderma tarandi (cattle botfly)[13]
6. Fannia (latrine fly) and alliphora, Lucilla, Sarcophaga, Gasterophilus, Callitroga, Cuterebra Dermatobia, Wohlfahrtia, Oedemagena, Chrysomya bezziana and Cochliomyia.[14]
Oestrus ovis larvae are the commonest cause of ophthalmomyiasis externa. Larvae of Dermatobia hominis, Chrysoma bezziana, Hypoderma tarandi, Cephenemyia trompe are found to be responsible for ophthalmomyiasis interna.[15]
Epidemiology
Ophthalmomyiasis is primarily seen in people working closely with animals, like people involved in animal husbandry and farmers.[16] The ophthalmomyiasis is commonly seen in tropical areas, especially in rural areas where hygiene is poor, with flies in abundance.[17] However, the disease can also present in people unrelated to the above-said working condition.[18][19][20]
At times accidental encounters with gravid female flies result in the darting of larvae into the conjunctival sac.[21] Cases of ophthalmomyiasis due to Oestrus ovis and Dermatobia hominis have been reported from India, Afghanistan, Iran, America, France, South Africa, and the Middle East.[22][23][24][25] Rhinoestrus purpureus and Rhinoestrus usbekistanicus are similar to Oestrus ovis and are responsible for external ophthalmomyiasis in Russia and Siberia.[26]
Most of the cases of ophthalmomyiasis are seen in the tropical and subtropical regions and are largely responsible for external ophthalmomyiasis. However, ophthalmomyiasis have also been reported from the Nearctic areas (northern Canada). The Hypoderma tarandi and Cephenemyia trompe are the flies responsible for ophthalmomyiasis interna and are primarily seen in Nearctic circumpolar regions. Other predisposing factors for ophthalmomyiasis are open surgical wounds, old age, debilitating conditions, and poor general health.[27]
Pathophysiology
The direct encounter with flies carrying larvae is the primary cause of ophthalmomyiasis externa. The flies drop the larvae over the ocular surface during this encounter. The most common cause of external ophthalmomyiasis globally is Oestrus ovis, and it reaches the human eye either by flies or by contaminated hands.[28]
Even for ophthalmomyiasis interna, the mechanism of reaching the ocular surface largely remains the same; however, in ophthalmomyiasis interna, cephaloskeleton and proteolytic enzymes secreted by the larvae may play an important role in ocular penetration. It is said that there exists a symbiotic relationship between the larva and the bacteria it carries. The larvae produce toxins and kill the tissues around and make the proteins available for proteolytic digestion by the bacteria. The proteolytic degradation, in turn, provides nutrition to the larvae.[29]
These facilitate penetration of the larvae intraocularly.[30] The point of entry is usually thought to be sclera.[29] The larvae can also reach ocular tissues via the hematogenous route.[31]
Histopathology
On histopathological examination of the larva, translucent to clear ovoid segmented structures are noted. Multiple rows of spicules at each segment and the terminal hooks are also noted on histopathological examination.[32] The larva also incites a foreign body reaction. It results in a non-necrotizing granulomatous reaction with dense infiltration by eosinophils (Spendore-Hoeppli phenomenon), and the larva can be seen covered with macrophages and foreign body giant cells.[33]
History and Physical
In ophthalmomyiasis, the patient will often have a history of working closely with animals like goats, sheep, reindeer, and caribou, depending on the geographical location.[30] In cases of external ophthalmomyiasis caused by Oestrus ovis, a history of the fly hitting the eye may be elicited. In external ophthalmomyiasis, the patient can present with signs and symptoms suggestive of acute bacterial or viral conjunctivitis.[34][35] The patient can have pain, itching, diffuse conjunctival hyperemia, lid edema, the sensation of something moving over the ocular surface, and multiple punctate subconjunctival hemorrhages with or without mucoid or watery discharge.[36]
The external ophthalmomyiasis caused by Dermatobia hominis results in eyelid nodular swelling simulating chalazion. The chalazion-like lesions have small larvae protruding from the center of the lesion on the palpebral conjunctiva.[37] The ophthalmomyiasis interna can be anterior or posterior depending on the presence of larva in the anterior or posterior segment of the eye respectively. The anterior ophthalmomyiasis interna is less common and presents with uveitis.[33] There are reports available on anterior segment involvement. Mobile larvae may be noted in the anterior chamber.[38] However, there is a potential threat of posterior migration.
The patients with ophthalmomyiasis interna often present with photopsia, pain, and floaters.[39] On examination, grayish-white subretinal tracks with or without exudative retinal detachment and vitritis can be seen. The larvae reach the vitreous cavity by penetrating the retina and inciting significant vitritis. Severe cases of ophthalmomyiasis interna can manifest as fibrovascular proliferation, focal hemorrhages, lens subluxation, and dislocation.[40] Disc edema can also be a manifestation of ophthalmomyiasis interna.[41] Other suggestive features like associated subretinal tracks or intravitreal larvae can help reach the final diagnosis.[42]
Orbital myiasis is considered the most dangerous, with a potential for intracranial spread. This is mainly seen in severely debilitated patients with uncontrolled diabetes mellitus, old age, and poor general health.[27] Orbital myiasis is a rapidly progressive condition and can destroy orbital tissues extensively within days.[43] The maggots often inhabit the open surgical or traumatic wound sites or ulcers. Other risk factors include rural background, alcoholism, stuporous condition, bed-bound status, poor self-care, poor hygiene, and malignant periorbital tumors.[44]
Evaluation
Patients with ophthalmomyiasis externa can be misdiagnosed as viral/ bacterial conjunctivitis. A thorough examination of the fornices is mandatory. The larvae of Oestrus ovis are photophobic and tend to hide in the fornices.[45] A good slit-lamp examination often reveals the diagnosis. The presence of multiple punctate hemorrhages can lead to an adenoviral conjunctivitis diagnosis. The hemorrhages are mainly due to microtrauma caused by the spines and hooks of the larvae in the absence of preauricular lymphadenopathy. The presence of a lid swelling with an associated history of wriggling movement warrants careful examination of the lid swelling with slit-lamp under high magnification. Chalazion-like lid swelling caused by Dermatobia hominis has a central hole through which larva can be seen.[37]
In cases of ophthalmomyiasis interna, a dilated fundus examination aids in the diagnosis. Clinically, multiple subretinal tracks can be seen, which are evident on optical coherence tomography as hypo-reflective areas.[46] Exudative retinal detachment and vitritis have also been reported. The Fundus Fluorescein Angiogram will show multiple hyperfluorescent subretinal tracks with or without leakage from the disc, depending on the presence or absence of disc edema.[47]
Fundus autofluorescence may reveal the subretinal tracks. For specific diagnoses, entomologists are involved. The first instar larva of Oestrus ovis contains hooks located more anteriorly attached to the cephalo-pharyngeal skeleton. For orbital myiasis, the imaging of orbit, brain, and paranasal sinuses is necessary. The larva should be sent for entomological examination in 70% ethanol.
Treatment / Management
The external ophthalmomyiasis is usually self-limiting.[35] However, for the early resolution of symptoms, the larvae need to be taken care of. The definitive management of external ophthalmomyiasis is the removal of the larvae from the ocular surface.[35] The ocular surface is anesthetized using topical proparacaine 0.5 or 0.4% xylocaine and using fine non-toothed forceps, and the larvae are removed.[48] A thorough examination of the ocular surface is done, including superior and inferior conjunctival fornices.[36] The patient is subsequently started on topical antibiotics and topical steroids.[49] The symptoms resolve following the removal of larvae. (B3)
Ivermectin 1% solution in propylene glycol and ivermectin with 0.6% povidone-iodine was used as a larvicidal agent in an in-vitro study. Both the agents are effective larvicidal agents; however, the ivermectin 1% solution with 0.6% povidone-iodine kills the larvae as early as 10 minutes.[50]
In cases of ophthalmomyiasis interna, a living subretinal larva can be killed by photocoagulation outside the macular area.[51] One can use an argon yellow laser of 330 mW power, 0.2 ms duration, and a spot size of 200 microns.[52] (B3)
In ophthalmomyiasis interna caused by onchocerciasis,[53] bancroftian filariasis, scabies, and strongyloidiasis single dose Ivermectin is very effective. Intravitreal maggot with significant vitritis needs to be removed by pars plana vitrectomy.[32] The immobile subretinal larva with significant inflammation needs pars plana vitrectomy and retinotomy.[54] Dead subretinal larvae with scars and without significant inflammation can be observed.[55] In cases with anterior chamber larva, emergent removal is advocated through a limbal incision to avoid posterior migration of the larva, which can occur rapidly.[38](B3)
The subretinal fly can sometimes exit the eye through the optic nerve. In the meanwhile significant decrease in vision can be noted. Treatment of optic nerve involvement with systemic ivermectin and steroids may help with visual restoration.[41] (B3)
Intracranial spread is the most feared complication of orbital myiasis.[56] To prevent intracranial spread, orbital exenteration is indicated.[57] In patients with poor general health and uncontrolled diabetes, strict glycemic control is recommended, along with adequate nutrition.[58](B3)
In orbital myiasis topical 4% xylocaine and turpentine oil, packing is indicated to immobilize the larvae. Subsequently, the larvae are removed manually. The patient is also started on oral and topical antibiotics.[59] Good hygiene and regular careful dressing of the affected area are crucial for recovery.(B3)
Differential Diagnosis
The ophthalmomyiasis externa mimics adenoviral conjunctivitis. The punctate hemorrhages due to microtrauma by larval spines are very similar to those seen in adenoviral conjunctivitis.
The anterior ophthalmomyiasis interna and anterior uveitis both present with severe anterior chamber reaction. However, in the anterior ophthalmomyiasis interna, the larva can also be seen in the anterior chamber.
The posterior ophthalmomyiasis can often be confused with isolated exudative retinal detachment. So a case of exudative retinal detachment should be thoroughly examined, especially in the endemic zones with a history of exposure.
Diffuse unilateral subacute neuroretinitis (DUSN) is an important differential diagnosis of ophthalmomyiasis interna (posterior). The subretinal tracts are usually thinner, and the causative organisms here are nematode larvae.[60] Here, there is dysfunction of both the inner and outer retina, though the larva resides subretinally.[61]
Usual presentation in the acute phase is vitritis, disc edema, and crops of white retinal lesions with possible detection of a moving nematode. Such nematodes must be neutralized by laser urgently as these may move rapidly and may be undetectable later. In the late phase, there are features of unilateral retinitis pigmentosa characterized by the pallor of the optic disc, retinal arteriolar attenuation, and pigmentary changes in the retinal periphery.[62]
Tunga penetrans (chigoe flea) burrow into the skin and may mimic Dermatobia hominis larvae.[63]
Prognosis
The external ophthalmomyiasis is a self-limiting condition and usually does not cause any significant damage to the ocular surface directly or cause any sequelae.[35] The ophthalmomyiasis externa has theoretical potential to become ophthalmomyiasis interna if not treated on time (not common with Oestrus ovis but common with Dermatobia hominis).[64] So, the condition needs to be treated at the earliest. In ophthalmomyiasis interna, the burrowing larva causes significant retinal damage along the subretinal tract it traverses. In cases of isolated identified subretinal larva, photocoagulation alone serves the purpose and has a relatively good prognosis.[51]
Despite extensive involvement of the retinal pigment epithelium, visual symptoms may be less, and good visual recovery is possible.[65] However, delayed diagnosis can lead to permanent visual loss and death in orbital myiasis cases due to the destruction of bone and meninges.[57] Even in patients with optic nerve involvement, the visual outcomes can be good if treated adequately and on time with single-dose systemic ivermectin (200 microgram/kg) and steroids (prednisolone 1mg/kg).[41]
Complications
The complications can vary from minor ocular symptoms to permanent visual loss. It can also cause disfigurement and can also cause death.[40] The ophthalmomyiasis externa has the theoretical potential to convert to ophthalmomyiasis interna.[42] The ophthalmomyiasis interna can lead to exudative retinal detachment, vitritis, lens subluxation, dislocation, and optic nerve invasion.[41] There is a risk of intracranial spread and subsequent death in orbital myiasis.[57]
Deterrence and Patient Education
The people working in close association with animals should be watchful about any ocular symptoms. They should consult ophthalmologists at the earliest if ocular symptoms arise. The development of ocular symptoms following an encounter with a fly should not be taken lightly.
Prevention has always been better than cure. Good personal hygiene can avert significant complications caused by ophthalmomyiasis. Previously efforts were made to let sterilized flies mate with fertile male flies in an attempt to control the ophthalmomyiasis outbreaks caused by flies. Ivermectin controlled-release capsules can also be used to prevent an animal infestation with bot fly and thus subsequent ophthalmomyiasis.[66] Considering this occupational hazard associated with animal rearers, specific measures need to be taken.
Enhancing Healthcare Team Outcomes
Ophthalmomyiasis can be treated efficiently and effectively if identified in time. Usually, the patients are from the countryside, and the earliest point of contact is vision center optometrists. The prompt identification of symptoms in high-risk groups should be referred appropriately to the ophthalmologists. Open communication between these professionals facilitates early identification and treatment of the condition and spreads awareness.
Awareness among healthcare workers serving in the areas with more commonly reported cases is the only way to mitigate the impact of the disease. Synchronized activity between sensitized health care workers and ophthalmologists can decrease morbidity significantly. Better communication between a parasitologist and the treating physician helps make an accurate diagnosis and can also help formulate a customized treatment depending upon the species identified.
Media
(Click Image to Enlarge)
Botfly larva over the hyperemic palpebral conjunctiva. Contributed by Prabhakar Singh
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