Ophthalmomyiasis Externa in a Puppy due to Cuterebra Infestation

Introduction

Ophthalmomyiasis is a term used to describe the invasion of mammalian ocular tissues by the larvae or eggs of flies in the order Diptera.¹ Various fly species represent this group of parasitic flies, including the genera Cuterebra, Hypoderma, Oestrus, Chrysomyia, and Dermatobia.² The effects of their infestation can be seen across many host species, including rodents, lagomorphs, ungulates, and even humans. Each fly species has a typical host species in which development occurs based on their geographic location and life cycle; however, atypical hosts are often accidentally parasitized, such as non-native rodents and lagomorphs, carnivores, ungulates, and primates.³

Ophthalmomyiasis can be further divided into three classes: externa (larval invasion of the ocular adnexa), interna anterior (larval invasion of the anterior chamber), and interna posterior (larval invasion of the posterior segment).^4,5 Ophthalmomyiasis is rarely reported in humans and tends to affect those persons in close contact with host species (e.g., sheep and cattle). The parasitic species most frequently reported to cause ophthalmomyiasis in humans are Oestrus ovis (external form), Hypoderma bovis (internal form), Dermatobia hominis, and Calliphoridae sp.^6–8 Although less frequently reported, Cuterebra infestations have also been documented in humans.^6–11

In dogs and cats, ophthalmomyiasis is rarely reported in the literature. There are only nine reported cases of ophthalmomyiasis interna in cats and two reported cases of ophthalmomyiasis interna in dogs.^4,5,12–17 There appears to be only one reported case of ophthalmomyiasis externa in a dog.¹⁸ In all reported cases of ophthalmomyiasis in dogs and cats, the larvae present were reported as Cuterebra species.

Cuterebra are host-specific, obligate parasites of various rodents and lagomorphs, with >30 species found across North America. Unlike many other Dipteran species, the adult Cuterebra has no functional mouthparts and does not directly bite or deposit eggs on its host. Eggs are deposited in the environment, often on vegetation surrounding the burrows of the target species. When an animal is in close proximity to the egg, the first-instar larva quickly hatches in response to the host's body heat. Once transferred to the typical host, the larva gains entry to the tissues (often via an orifice, wound, or the eyes) and spends the next week or so migrating until it localizes in subcutaneous tissue to continue its maturation. The larva establishes a pore through which to respirate and void excrement and then molts to the second-instar stage. The larva feeds on the host's interstitial tissue and blood as the host forms a capsule around the parasite composed of collagen, connective tissue, and inflammatory cells (i.e., a “warble”). Eventually, the larva matures to the third-instar stage, which can be as large as 3 cm long and 1 cm wide. The larva reaches maturity in approximately 30 days, at which time it exits the host and pupates in the environment to hatch the following year. The remaining open wound (warble) closes a few days after the larva exits the pore and usually heals without incident in 1–2 wk.^1–3

A similar process occurs when a Cuterebra larva enters an atypical host; however, significant differences can exist in both the host and larval responses when this occurs. Incomplete life cycles, poorly developed warbles, and alterations in migration patterns are potential problems that affect the larvae in atypical hosts.³ The hosts themselves are not adapted to carrying these parasites and therefore tend to have more severe complications when infested. Complications in atypical hosts that have been reported include temporary paralysis during larval migration, aberrant migration (invasion of respiratory, cerebrospinal, and ocular tissues), nutritional deficits, and poorly healing or infected warble (warble sites).^{3–5,12–17,19,20}

This report describes the diagnosis and treatment of ophthalmomyiasis externa in an atypical host due to Cuterebra infestation. This is the second report to do so; however, it is the first report of ophthalmomyiasis externa involving the eyelid margin, a unique location of the warble pore in this case.

Case Report

An 8 wk old, intact, female Scottish terrier puppy weighing 1.67 kg (3.67 lbs), presented to Kansas State in early July for a growing eyelid mass of 2 wk duration. The patient had originally presented to the referring veterinarian for a focal cellulitis and puncture wound near the lateral canthus of the right eye. The veterinarian prescribed an ophthalmic neomycin-polymyxin B-bacitracin combination antibiotic ointment q 6 hr. Over the next 2 wk, the wound continued to produce copious amounts of blood-tinged mucopurulent discharge, and the focal area of cellulitis slowly increased in size, taking on the appearance of a mass. The enlarging mass caused the globe to shift medially and the owner began noticing frequent blepharospasms. During this 2 wk time period, the puppy became lethargic and was not competing with littermates for time to nurse. Upon showing evidence of weight loss and stunted growth, the owner began bottle feeding the puppy separately. The puppy appeared to return to a more normal body condition, although her activity level remained diminished.

On presentation to Kansas State, the puppy was bright, alert, and responsive, although not overly exuberant. The puppy had a body condition score of 4/9 and was adequately hydrated. No other abnormalities were noted on general physical examination. Ocular examination revealed a 2×2 cm mass present at the lateral canthus of the right eye (OD). The mass appeared to involve the lateral canthus, conjunctiva, and adjacent upper and lower eyelids. At the center of the mass, a circular pore was noted with copious mucopurulent discharge and evidence of previous hemorrhage. Upon closer examination, the mass appeared to be pulsating, and the pore was found to contain two symmetrical spicules. Removal of the discharge revealed a well-developed larva present in the lateral aspect of the orbital cavity, anchored at the lateral canthus of the OD (Figure 1). The normal canthal anatomy was disrupted by the circular pattern of the pore itself, and the eyelid margins were no longer congruent. The right globe was severely displaced ventromedially by the mass effect produced by the growing larva and was unable to be assessed. Examination of the left eye (OS) revealed iris to iris persistent pupillary membranes, a normal Schirmer Tear Test^a (19 mm/60 sec; >15 mm/60 sec considered normal), and no fluorescein stain^b uptake. Differential diagnoses considered for the right lateral canthal mass included external ophthalmomyiasis (Cuterebra spp., Hypoderma spp., or Oestrus ovis), abscess, or foreign body. External ophthalmomyiasis was confirmed upon visualization of larval spicules, cuticular spines, and pulsating movements generated by the parasite.

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A packed cell volume (34%; reference range, 29–33.8%), total solids (5.0 g/dL; reference range, 5.0–6.5 g/dL), blood glucose (111 mg/dL; reference range, 73–113 mg/dL) were performed in preparation for anesthesia. The patient was premedicated with diazepam^c (0.2 mg/kg intramuscularly [IM]) and butorphanol^d (0.2 mg/kg IM) and induced with propofol^e (9 mg/kg IV, to effect) and maintained on an oxygen-isoflurane^f gas mixture for the duration of the procedure. One dose of ampicillin-sulbactam^g was administered (20 mg/kg IV) before the start of surgery. The area around the lateral canthus was clipped and prepared with a dilute povidone iodine solution^h. The larva was then grasped with tissue forceps and extracted with gentle traction to avoid damaging the larva, causing release of internal larval contents. A large, intact larva was extracted from the orbital cavity and placed in formalin for identification (Figure 2). Copious amounts of saline were used to flush the warble cavity of debris, revealing a large defect in the right orbit (approximately 1×2 cm) surrounded by a thick fibrous capsule. The margins of the wound were debrided, focusing on the tissue directly adjacent to the lateral canthus and eyelid margins. The lateral canthus was repaired with 5-0 polyglactin 910 sutureⁱ using four simple interrupted skin sutures. The first suture recreated the lateral canthus by apposing the upper and lower eyelid margins in proper conformation and was located on the epidermal surface just lateral to the canthal margin. Additional, evenly spaced sutures were placed to close the skin defect.

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Postoperatively, the patient was prescribed 1% ofloxacin^j ophthalmic solution (1 drop OD q 6 hr for 14 days), meloxicam^k (0.1 mg/kg per os [PO] q 24 hr for 3 days), and amoxicillin-clavulanic acid^l (14 mg/kg PO q 12 hr for 14 days). An Elizabethan collar was placed on the patient to protect the canthotomy repair, and she was discharged from the hospital the next day. The globe remained ventromedially displaced in the orbit at the time of discharge from the hospital.

The larva was submitted to the Kansas State University Veterinary Parasitology Diagnostic Laboratory for identification. The larva measured 2.2 cm long and 1.1 cm wide. The cuticle was a dark brown color and was covered in dark, conical spines. It was identified as a third instar larva of the Cuterebra sp. based on characteristic size, color, and appearance, and arrangement of spines (Figure 3).^21,22 The patient returned 10 days later for reevaluation and suture removal. At that time, the puppy was bright, alert, and responsive, and more active during examination than the previous visit. Physical examination revealed no abnormal findings. The skin sutures were removed. Ocular examination revealed a healed lateral canthus with good apposition and mild alopecia noted along the incision line. The overall cosmetic outcome was excellent (Figure 4). The right globe had returned to normal position, had normal ocular motility, and normal retropulsion. The patient navigated well through the room and could follow cotton balls readily. The patient lacked a menace response, which was expected, as this is a learned response and is generally not present in puppies of her age. Intraocular examination of the OD revealed persistent pupillary membranes. No remaining conjunctival wound could be found. Normal Schirmer Tear Test^a values (15 mm/30 sec OD, 24 mm/60 sec OS) and intraocular pressures^m (13 mm Hg OD, 11 mm Hg OS) were noted in both eyes. There was no fluorescein stain^b uptake in either eye. The puppy was released to the owner with no further treatments necessary. The dog was not examined again after being sold to a new owner who lived out of state.

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Discussion

In this case, a third-instar Cuterebra larva was found inhabiting the orbital cavity and adjacent adnexal tissues. The larva was nearly fully mature, with a well-developed cuticle covered in spines. The time of year was consistent with the predicable seasonal occurrence of Cuterebra infestation, which lasts from late spring until fall.¹ The owner noticed a “bite wound” present 2 wk before presentation, which was presumed to have been acquired during various incidences of rough housing among the puppies. Though Cuterebra larvae have been observed to enter through wounds,²³ the mature state of the larva 2 wk after the initial wound was noticed suggests an earlier presence. Either the warble pore had just been established at the time of initial presentation to the referring veterinarian or the pore had finally grown to a more noticeable size. In either case, the larva had likely developed to the second- or third-instar stage by the time the wound was recognized by the owner. As an atypical host, the puppy was likely infested while investigating her environment in the 1–2 wk before the first signs of disease. Discussions with the owner revealed the patient had access to the outside environment, including areas of unkempt natural habitat likely to house local rodent or lagomorph species.

Definitive speciation was not obtained for the larvae in this case, as classification of the adult fly would be required; however, cuticular platelet characteristics (raised, mostly single-pointed, spine-like platelets) suggested it could have been of the lagomorph variety (Figure 5).^24,25 The lagomorph-infesting Cuterebra species with a known home range within the patient's environment of eastern Kansas include C abdominalis, C rufricus, C buccata, and C jellisoni.² Of those species, C jellisoni is known to have a site preference in the tissues of the head in its typical host, including the areas around the eyes.²³ Site preference has been witnessed in other Cuterebra species; however, this patient represented an atypical host. ²³ As discussed earlier, migration and maturation are often abnormal when the infestation occurs outside of the typical host species, suggesting that speciation based on warble site specificity would be difficult to prove in this atypical host.

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The systemic implications of living as an active host of the larva are clear in this patient. According to the owner, the patient seemed thinner than other litter mates, was lethargic, and was unable to compete for time nursing, suggesting this was related to the discomfort and nutrient loss created by the large, mature larva. When given supplemental feedings by the owner, the patient gained weight and continued to thrive. To better understand any possible systemic effects on the patient, complete blood count and blood chemistry profile could have been performed. Due to the relative health of the puppy and lack of systemic clinical signs at the time of presentation, these diagnostics were not pursued (although the packed cell volume, total solids,and blood glucose were performed in preparation for anesthesia and were within normal limits).

The treatment recommended for Cuterebra infestation is manual removal with forceps. Asphyxiation can also be attempted by placing petroleum jelly over the respiratory pore of the larva, forcing it to exit to respirate.⁸ It is important to remove the larva in its entirety and take every precaution to not macerate the cuticle when it remains in the host, as exposure to internal larval contents can reportedly cause anaphylaxis or severe hypersensitivity reactions.¹⁹ To facilitate removal, a 2% solution of lidocaine can be used to paralyze the larva.⁷ When the parasite is located elsewhere in the body, the host animal is often awake or mildly sedated when the larva is removed. For our patient, the decision to place the animal under general anesthesia was made due to the proximity of the larva to the globe and the necessity for lateral canthus repair after larva removal.

As discussed earlier, empty warble sites tend to heal quickly and without complication in typical host animals. In atypical hosts, healing can be delayed and secondary bacterial infections have been observed.³ In this case, the location of the warble necessitated minor debridement to facilitate proper apposition of the eyelid margins; however, the majority of the cavity was left to heal by second intention. The cavity was located primarily in the vascular conjunctival and orbital tissues, which have excellent healing potential. The orbital tissues were displaced by the fibrous capsule of the warble, and ocular anatomy was difficult to assess at the time of surgery. Aggressive debridement of affected tissues might have compromised the normal tissues and was deemed unnecessary. The heavy purulent discharge present at the time of presentation could have represented a secondary bacterial infection or a vigorous atypical host response to the presence of the parasite. Cytology or culture of the effected area could have been performed to identify a bacterial infection and help direct antibiotic therapy, although they were not performed in this case in favor of empirical treatment with topical and systemic antibiotics.

Conclusion

External ophthalmomyiasis is uncommon in domesticated pet animals; however, exposure to typical host animal environments increases the risk of infestation. Cuterebra larval infestation can be recognized by its characteristic wound appearance, subcutaneous swelling, and warble pore, with or without a purulent discharge. The time of year and important historical clues can also aid in diagnosis. Due to the close proximity to important ocular structures, it is recommended to carefully remove the larva manually and correct any important conformational defects. The warble cavity proper can be left to heal by second intention; however, antibiotic therapy is recommended in atypical hosts due to higher rates of secondary infection.^1,3,18,23