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Trauma-Induced Uveitis and Free Air in the Anterior Chamber of Three Eastern Screech Owls (Megascops asio).

Abstract: Unusual ocular abnormalities were documented in 3 wild eastern screech owls (Megascops asio) presented to a wildlife rehabilitation hospital after vehicular strike-induced trauma to the head. All 3 had anterior uveitis and free air bubbles in the anterior chamber, but none of the cases had any discernable corneal damage, either grossly or with fluorescein stain technique. Perforation of the globe at the level of the scleral ossicle was considered a possible cause. All 3 cases recovered with standard treatment for anterior uveitis, and the free air was absorbed within 10-14 days and did not appear to cause any lingering complications. The owls were later released back into the wild after demonstrating the ability to navigate obstacles in a flight cage and capture live prey.

Key words: ocular trauma, anterior chamber, uveitis, air bubble, avian, eastern screech owl, Megascops asio

Clinical Report

Three adult eastern screech owls (Megascops asio) of unknown sex and age presented to a wildlife hospital and rehabilitation center in southwest Florida over a 3-year period (2013-2015). All had a history of known or strongly suspected vehicular strike trauma, having been found on or beside major roadways.

Case 1

Pertinent findings on physical examination of this owl were mild abrasion of the cere, a dark spot behind the left tympanum consistent with clotted hemorrhage in the inner ear, and ocular abnormalities of the left eye (OS). Body weight (BW) was 115 g, and body condition score was recorded as 3/ 5. Neurologic examination revealed depressed mentation but otherwise appeared normal for a screech owl under daylight conditions. The patient had a more complete ocular examination in a dark room with a direct ophthalmoscope. The right eye (OD) appeared within normal limits in both anterior chamber and fundus. However, hyphema, mild aqueous flare consistent with anterior uveitis, and 2 air bubbles in the anterior chamber (Fig 1 A) obscured the left pupil, precluding fundic examination on that side. The patient had mild blepharospasm OS, but fluorescein stain did not show any dye uptake in either eye. A Schirmer tear test (STT) showed roughly equal tear production on both sides, at 2.3 mm/min. A drop of proparacaine hydrochloride ophthalmic solution 0.5% was placed in each eye, and the intraocular pressure (IOP) was assessed by applanation tonometry (Tono-Pen XL, Reichert Technologies, Depew, NY, USA). Pressures were recorded as 8 and 10 mm Hg OS and OD, respectively. Perforation of the left globe was suspected on the basis of free air in the anterior chamber of the eye, but survey radiographs revealed no obvious fractures of the orbit. The owl was treated with a hetastarch bolus (10 mL/kg IV over 10 minutes), crystalloid fluids (lactated Ringer's solution, 100 mL/kg SC in the prefemoral web) and buprenorphine (0.6 mg/kg IM q8h), meloxicam (0.5 mg/kg IM ql2h), and ceftiofur (10 mg/kg IM q72h), all in the pectoral musculature, within 15 minutes of admission to the hospital. Additionally, the patient was given flurbiprofen (1 drop OS q8h) and triple antibiotic ointment (neomycin, polymyxin B, bacitracin; OS q8h) and placed in an oxygen ([O.sub.2]) cage at 98% [O.sub.2] overnight. On day 2, the owl remained in ventral recumbency on the cage floor and was depressed and inappetant, with no ocular changes from presentation, so assisted alimentation with a liquid critical care diet (Emeraid Intensive Care Carnivore, Lafeber Co, Cornell, IL, USA) at 5% of BW was instituted 3 times daily by gavage. By day 3, the owl was more alert and was removed from oxygen. The buprenorphine, parenteral meloxicam, and fluids were discontinued, and the patient started on tramadol (20 mg/kg PO q8h) and meloxicam (0.5 mg/kg PO ql2h) and was assist-fed with soft mouse pieces. All other medications were continued as on day 1. No changes were noted OS, and IOPs remained in the 7-9 mm Hg range, consistent with mild uveitis. The owl began eating mice left in the cage on day 5 and mentation appeared normal. Ophthalmic examination OS revealed a more organized blood clot in the anterior chamber, the smaller air bubble had resorbed, the larger air bubble appeared subjectively smaller, and the uveitis had improved. A small portion of the retina was visible and appeared normal. The IOPs were within the normal range at 11 mm Hg. By day 7, the patient was eating well, muting and casting normally, maintaining BW, and no longer demonstrating any blepharospasm OS and so was moved to an outdoor flight cage. Oral medications were continued by being placed in prey items, which the patient ate twice daily. All ocular medications were discontinued. By day 10, the air bubbles in the anterior chamber had completely resolved, although a small blood clot remained in the anterior chamber and possible anterior (iris to cornea) synechiae were forming. A fundic examination revealed a small area of hemorrhage in the retina that was well organized, and IOPs continued to be within reference limits in both eyes. The owl was able to fly around vertical obstacles in the cage and catch live prey items. All medications were discontinued. By day 14, a small area of anterior synechiae had formed and was compromising the ability of the iris to have complete contraction even outdoors in the bright sunlight. However, because screech owls are predominately nocturnal, and because IOPs continued to be within the normal range, this was not felt to be an impediment to release. The owl was successfully released back to the location where it was found that night.

Case 2

Pertinent findings on physical examination of this owl were obtunded mentation and ocular abnormalities OS, including blepharospasm. The BW was 121 g, and body condition score was 3.5/5. On complete ocular examination, mild conjunctival hyperemia and episcleral injection were noted, with moderate aqueous flare, corneal edema and iridal hyperemia (rubeosis iridis) consistent with anterior uveitis, and 5 small air bubbles (Fig IB). The posterior segment OS was not able to be visualized. The right eye and ipsilateral aural area were considered normal. A STT was not performed. Fluorescein stain did not show dye uptake in either eye. A drop of 0.5% proparacaine hydrochloride ophthalmic solution was placed in each eye, and IOP was measured by applanation tonometry. Pressures were recorded as 6 and 11 mm Hg OS and OD, respectively, consistent with the anterior uveitis OS and possible perforation of the left globe. Radiographs were not done at admission because of the critical status of the patient.

A 24-guage IV catheter was placed in the right jugular vein and kept in place with an adhesive transparent dressing over the catheter site, with no circumferential bandaging around the neck. The owl was treated with mannitol (0.5 g/kg IV over 15 minutes) followed by a hetastarch bolus (10 mL/kg IV over 15 minutes), then placed on continuous rate infusion of crystalloid fluids (lactated Ringer's solution, 100 mL/kg) over the next 24 hours. Additionally, the patient received buprenorphine (0.6 mg/kg IM q8h,) ceftiofur (10 mg/kg IM q72h), prednisone acetate 1% ophthalmic solution (OS q8h), ofloxacin 0.3% ophthalmic solution (OS q8h) and was placed in sternal recumbency with the head elevated approximately 30[degrees] in an oxygen cage at 98% [O.sub.2]. The next day, the owl was standing, but mentation was still significantly depressed. Treatment was continued as described on day 1, except the mannitol was discontinued. The patient had not eaten since admission, so assisted alimentation (Emeraid IC Carnivore) by gavage was instituted 3 times daily. On day 3, the owl was more alert, so the IV catheter was removed, the buprenorphine discontinued, and treatment with tramadol (30 mg/ kg PO q8h) begun. The bird still had blepharospasm OS, although clinical signs of uveitis were less pronounced. Repeated IOPs showed mild improvement to 8 mm Hg OS and were still within normal limits OD. Force feeding with soft mouse pieces was begun and gavage feeding was discontinued. Radiographs were taken on day 4 under general inhalant anesthesia and revealed no significant findings. At this time, a fundic exam was able to be done, and an area of retinal detachment was noted affecting approximately 20% of the peripheral portion of the retina medioventrally, but the area around the fovea was unaffected.

The patient gradually improved and was moved to an outdoor flight cage on day 7, and all medications were discontinued, despite still having a small amount of air in the eye and some apparent vision deficits OS. Unfortunately, the next day the owl was noted to have blepharospasm again OS. At this time, fluorescein stain OS revealed a small corneal ulcer. The owl was rehospitalized and ofloxacin drops restarted as before. Over the next 3 days, the ulcer did not improve, and on day 11, a drop of proparacaine was applied OS, and a sterile Dacron-tipped applicator was used to debride the ulcer. Cytology showed a few gram-positive cocci and numerous inflammatory cells. Topical medication was changed to neomycin/polymyxin B sulfate/gramicidin ophthalmic solution (OS q6h) and 1 drop of serum (OS q6h) from a great horned owl (Bubo virginianus) donor. The ulcer healed without incident over the next 3 days, and the last of the air and corneal edema also resolved. The owl was moved to a flight cage and was observed on remote camera to be flying, avoiding obstacles, and catching live prey items. The owl was released on day 30 after admission with normal IOPs, no further corneal ulcers, complete resolution of the uveitis, and estimated 40%-50% improvement of the retinal detachment.

Case 3

Pertinent findings on physical examination of this owl were depressed mentation, hemorrhage in the left ear, and blepharospasm OS. The BW was 125 g and the body condition score 3/5. Complete ocular examination noted hyphema, mild aqueous flare and iridal hyperemia consistent with anterior uveitis, and 1 air bubble in the anterior chamber OS (Fig 1C). The posterior segment of both eyes showed a mild (OD) to moderate (OS) amount of retinal hemorrhage, but the portions of the retinas not obscured by blood appeared normal. A STT showed 2.9 mm/min OD and 2.3 mm/min OS. Fluorescein stain did not show any dye uptake in either eye. A drop of proparacaine hydrochloride 0.5% ophthalmic solution was placed in each eye, and intraocular pressure was assessed by applanation tonometry. Pressures were recorded as 4 and 9 mm Hg OS and OD, respectively, consistent with the anterior uveitis and possible perforation of the left globe. Although perforation of the globe was suspected, survey radiographs did not reveal any definitive fractures of the skull, scleral ossicles, or orbit. The patient's status declined during physical examination, with the owl becoming less responsive to any stimuli. An intraosseous (IO) catheter was placed in the right distal ulna, a shock bolus of room temperature crystalloid fluids was given (45 mL/kg per hour), and the patient was placed in an oxygen cage at 98% [O.sub.2]. After 1 hour, the owl was slightly more responsive but still depressed. At this time, hypertonic saline (3 mL/kg IO over 10 minutes) was given, later followed by hetastarch (10 mL/kg IO over 15 minutes) via syringe pump while still in the oxygen cage. The patient was ventrally recumbent and was kept with its head elevated approximately 30[degrees]. Treatment was initiated with crystalloid fluids (75 mL/kg per day), hydromorphone (0.3 mg/kg IM q8h), ceftiofur (10 mg/kg IM q72h), flurbiprofen (1 drop OS q8h), and ofloxacin 0.3% ophthalmic solution (1 drop OS q8h). The next day, the patient was more responsive but still recumbent, so the hydromorphone was discontinued, and tramadol (30 mg/kg PO q8h) and meloxicam (1 mg/kg PO q12h) were added to the treatment protocol. Parenteral fluid therapy was discontinued, and the IO catheter was removed. The owl was started on gavage feeding (Lafeber IC Carnivore) at 5% of BW. The left eye was unchanged, and IOPs remained low. By day 5, the air bubble in the anterior chamber was smaller, but both anterior and posterior synechiae began forming, rendering the pupil an abnormal shape and incapable of contraction or dilation (Fig 1). Nonetheless, it was believed that some degree of vision still existed in the left eye. After 9 days, the air had resorbed from the anterior chamber and the blood clots in the retina and anterior chamber were partially resorbed. The owl was placed in an outdoor flight cage, and all medications were discontinued. The owl appeared to navigate normally and was seen catching live roaches on closed-circuit camera. It was subsequently released after 15 days.


To our knowledge, this is the first published report of trauma-induced free air bubbles in the anterior chamber of any avian species. Owls, compared with mammals, have large eyes relative to body size. The globe is located in an incomplete orbit and is supported by small, bony plates within the sclera known as scleral ossicles. The presence of scleral ossicles helps to prevent collapse of the globe, even if it has been ruptured. The shape of the globe is determined by these ossicles and is uniquely tubular in owls (Fig 2). An elongated convexity to the ciliary region toward the posterior region of the globe maximizes light capture in dim lighting conditions. There is little room for anything other than the globe in the tight-fitting orbit, and extraocular muscles are so negligible as to be almost vestigial. The eyelids are thin, and the lower lid is less mobile in owls than the upper lid. The third eyelid is transparent to allow for its dispatch, even during flight, without interfering with vision. In the owls we describe, all adnexal structures appeared normal.

In a raptor with a history or physical examination findings consistent with trauma, thorough examination of the eyes, including the posterior segment whenever possible, is crucial. Blind birds are not releasable, but they also may not be kept in captivity under federal law. Some retrospective studies report anywhere from 30% to 75% of all traumatized raptors suffer from ocular lesions. (1-5) Additionally, 88%-90% of eye disorders diagnosed in wild raptors are attributed to trauma. (1,6) Bilateral injuries were more common than unilateral injuries in at least 1 study of 2 owl species. (4) In this same study, 8% (6/74) of ocular lesions involved the anterior segment alone, 43% (32/74) the posterior segment alone, and 49% (36/74) both segments in little owls (Athene noctua), whereas 39% (19/49) involved the anterior segment alone, 16% (8/49) involved the posterior segment alone, and 45% (22/49) involved both segments in Eurasian scops owls (Otus scops). (4)

The head should be examined from every angle looking for asymmetry. Checking the ear canals is also important, both because any sign of trauma in the ear may suggest ocular posterior segment trauma and because owls rely heavily on auditory cues during hunting. (7) If both visual and auditory damage are observed, then prognosis for release may be downgraded. Menace response is not always accurate in avian species. Mild anisocoria might be normal, but consistently unequal or fixed pupils may indicate disease. Direct pupillary reflexes are difficult to evaluate because of the presence of striated muscle in the iris. Indirect pupillary reflexes are not expected in birds because of the complete decussation at the optic chiasm. Contralateral miosis may be a consequence of direct stimulation of the optic nerve through the thin interorbital septum. Ocular structures in the anterior segment should be examined by use of frontal and lateral illumination, preferably with magnification, or with at slit lamp.

The history of blunt force trauma (ie, vehicle strike), normal BW and condition scores, free air in the anterior chamber, and decreased IOPs in the affected eyes in these cases are most consistent with acute perforation of the globe. Because initially no corneal ulceration was evident, most likely, perforation of the globe occurred at the level of the sclera behind the lid margins, possibly from a fractured scleral ossicle (Fig 3). Fractured scleral ossicles have been reported in 1 raptor case previously. (8) Although periorbital fractures were not visible in any of these cases radiographically, the level of detail in a minimally displaced fracture may not have been appreciable with standard digital radiography. Computed tomography or ultrasound may have been a more sensitive imaging modality but was not performed in these patients. (9) In all cases, the air resorbed and IOPs returned to levels within established reference ranges for eastern screech owls. (10) In the second and third cases, which developed synechiae, an argument might be made that obstruction of aqueous flow could occur at both the pupil and iridocorneal angle, which might later lead to glaucoma. (11) However, birds have a wide drainage angle, and because IOPs remained stable over several weeks of hospitalization, the decision was made to release the patients. (12)

Hyphema has been identified as one of the most common traumatic ocular lesions seen in wild raptors. (1,4) Its presence indicates that the eye has suffered a significant injury, and structures within the anterior and posterior segments are likely to be affected. (13) Hyphema was seen in all 3 owls, and use of tissue plasminogen activator via intracameral injection for improved lysis of blood clots may have helped to prevent synechia formation. However, this was not done in these cases because there is little published information on use in avian species. Tissue plasminogen activator is most effective when used within hours of hemorrhage and production of fibrin but should not be used with active hemorrhage, as it can potentiate bleeding. (14)

Air alone (in small amounts) should not be harmful to the anterior chamber and should be absorbed within a few days, as seen in these cases. If the air represents penetration of the globe, however, then secondary uveitis can be expected. In people, air may be injected into the anterior chamber at the end of surgery as a tamponade to prevent the chamber from shallowing for the first 1-2 days after surgery. Surface tension and buoyancy of the bubble may help to maintain the space between the cornea, iris, and lens. (15) Air bubbles are also injected into the anterior chamber for treatment of Descemet's membrane tears after cataract surgery, (16,17) for prevention of endophthalmitis due to Staphylococcus epidermidis, (18) for treatment of corneal hydrops in keratoconus, (19) and during deep lamellar endothelial keratoplasty in humans. (20) One study in pigs showed that an artificially introduced air bubble in the anterior chamber will not necessarily cause any changes in IOP. (21) Some studies in rabbits have shown that when an air bubble is left in the anterior chamber after cataract surgery, it reduces inflammation. (22,23) However, free air in the anterior chamber has caused further complications in cases in humans, principally in glaucoma. (24,25)

Whenever an owl has vision deficits in an eye, that eye may be more predisposed to corneal ulcers because the surface of the eye is quite large, and the decreased ability for the animal to visualize objects may create the potential for ocular trauma. (26) However, some studies have suggested that owls with vision deficits or even blindness in 1 eye do have the capacity for survival. (12,27) Owls have a single fovea located superior and temporal to the pecten body. Although the owl in case 2 did sustain retinal damage, the fovea was unaffected, and vision appeared to be sufficient for normal activity.

The STT and red phenol thread test have been validated for multiple avian species. (2,28-31) Strigiformes show low values normally because they have small lacrimal glands, so assessment of tear production using the standard STT may be more difficult. Although tear production was only measured for cases 1 and 3 in these eastern screech owls, measurements appeared to be normal based on reference ranges established in 1 study with tawny owls (Strix aluco), where reported mean values were 5.6 [+ or -] 3.3 mm/60 s for the STT and 19.3 [+ or -] 5.8 mm/15 s for the red phenol thread test. (28) Thus, having free air in the anterior chamber did not appear to have any demonstrable effect on tear production in 2 cases.

Intraocular pressure can be measured by applanation tonometry in corneas larger than 9 mm in diameter, whereas rebound tonometry may be a better alternative in individuals with smaller corneas. (32) Mean corneal dimensions for eastern screech owls have been reported to be 14.5 [+ or -] 0.5 mm vertically and 15.25 [+ or -] 0.5 mm horizontally, with IOP reference ranges of 11 [+ or -] 1.9 mm Hg with the Tono-Pen XL device. (10) Standard IOP reference values in raptors with the TonoVet (Icare, Vantaa, Finland) rebound tonometer vary from species to species but are generally in the 10-25 mm Hg range, using the instrument's "d" or dog setting, but trend toward the lower end of that range in nocturnal birds. (10,30-35) In these cases, applanation tonometry was used and demonstrated IOPs that were within reference ranges in the unaffected eyes, with decreased IOPs in the affected eyes.

The classic signs of uveitis are the same in birds as they are in mammals--aqueous flare, hypopyon, corneal edema, and nonspecific findings, such as blepharospasm or enophthalmos with third eyelid elevation. (34-36) A common cause of uveitis in wild birds is blunt trauma and thus is seen frequently in raptors. (27) Topical corticosteroids or nonsteroidal anti-inflammatory drugs, sometimes used in conjunction with systemic nonsteroidal anti-inflammatory drugs, are usually quick to resolve the problem. However, unlike most mammalian species, retinal detachment after blunt trauma is relatively common in birds, especially raptors, so thorough examination of the posterior segment should be done as soon possible. The avian retina is anangiotic (no visible blood vessels) and generally believed to be atapetal (except in Caprimulgiformes). Nocturnal birds have less pigmented retinas than diurnal ones, and young owls, in particular, have very little pigment. Being familiar with the normal anatomy for the species under examination can greatly enhance recognition of abnormalities.

Chorioretinitis is a common sequela of blunt ocular trauma in birds and often presents concurrently with anterior uveitis. (35,36) Therefore, even if a fundic examination is not immediately possible, it may be indicated to initiate treatment for chorioretinitis (ie, systemic anti-inflammatory drugs). Systemic steroids are rarely indicated in avian species and may cause severe immunosuppression. However, a single injection of short-acting steroids has been recommended by some in cases of chorioretinitis in birds. (12)

Disruption of the corneal epithelium with variable loss of the corneal stroma constitutes corneal ulceration. Typical signs manifested by affected birds include acute, unilateral blepharospasm and epiphora. Anisocoria from reflex uveitis may result in miosis of the affected eye, but it is less commonly seen in birds because of their voluntary control of pupil size. Other clinical signs to be aware of when evaluating a bird with corneal ulceration are variable degrees of aqueous flare (anterior uveitis), depending on the ulcer's severity and duration; variable degrees of corneal edema; and fluorescein stain uptake that will adhere to any exposed corneal stroma and is an essential diagnostic tool to delineate fully the ulcer's extent. In these cases, corneal ulceration was not documented on admission, so the tear in the globe must have occurred posterior to the lid margins. Ocular ultrasound and electroretinography may be helpful when anterior segment disease (eg, severe corneal edema, hyphema, or both) preclude adequate intraocular examination, especially if a concurrent retinal detachment or lens capsule rupture is suspected. (9) However, these procedures may cause additional damage in acute trauma cases and were not pursued in these birds. An interesting feature of these cases was the free air in the anterior chamber with no obvious corneal ulceration.

Heather W. Barron, DVM, Dipl ABVP (Avian), Julia M. Hill, DVM, Kristen M. Dube, BVMS, MRCVS, Jennifer L. Riley, DVM, Robin L. Bast, DVM, Brittany N. Stevens, DVM, and Lorraine G. Karpinski, VMD, Dipl ACVO

From the Clinic for the Rehabilitation of Wildlife. 3883 Sanibel-Captiva Road, Sanibel, FL 33957, USA (Barron. Hill. Bast); the Phillip and Patricia Frost Museum of Science, 1101 Biscayne Boulevard. Miami. FL 33132. USA (Dube); the Blue Ridge Wildlife Center. 106 Island Farm Lane. Boyce, VA 22620, USA (Riley); the Department of Veterinary Medicine and Epidemiology, University of California Davis, School of Veterinary Medicine. One Shields Avenue. Davis. California 95616. USA (Stevens); and the Pinecrest Veterinary Hospital, 12125 South Dixie Highway. Miami. FL 33156, USA (Karpinski).


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Caption: Figure 1. Images taken on admission of the left eye of 3 adult eastern screech owls with a history of blunt force trauma resulting in free air and uveitis in the anterior chamber. Case 1 (A), Case 2 (B), and Case 3 (C).

Caption: Figure 2. Illustration of scleral ossicles in an eastern screech owl shows how they help to prevent collapse of the globe, even if it has been ruptured. The shape of the globe is determined by these ossicles and is uniquely tubular in owls.

Caption: Figure 3. Air in the anterior chamber of 3 eastern screech owl eyes may have occurred from a fractured scleral ossicle (arrow), leading to perforation of the globe at the level of the sclera behind the lid margins.
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Title Annotation:Clinical Report
Author:Barron, Heather W.; Hill, Julia M.; Dube, Kristen M.; Riley, Jennifer L.; Bast, Robin L.; Stevens, B
Publication:Journal of Avian Medicine and Surgery
Date:Dec 1, 2018
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