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Normal ocular parameters and characterization of ophthalmic lesions in a group of captive bald eagles (Haliaeetus leucocephalus).

Abstract: Sixteen adult captive bald eagles (Haliaeetus leucocephalus) underwent a complete bilateral ocular examination to assess normal ocular parameters and describe ophthalmic lesions. Tear production was measured with the Schirmer tear test 1 and intraocular pressure was measured with applanation tonometry. The menace response was normal bilaterally in 13 of 16 eagles. Two birds had normal menace responses despite having fundic lesions, and 2 birds with an inconsistent or absent menace response did not have appreciable ophthalmic lesions. Mean (SD) tear production was 14 [+ or -] 2 mm/min (range, 8 19 mm/min). Mean intraocular pressure was 21.5 [+ or -] 1.7 mm Hg (range, 15-26 mm Hg). At least 1 ocular lesion was present in 50% of examined eyes. Cataracts, the most common lesion observed, were present in 8 eyes of 5 birds. Three of 4 known geriatric birds were or had been affected with bilateral cataracts. Overall, ocular lesions are common in captive bald eagles, and cataracts appear to be more prevalent in geriatric bald eagles. An obvious positive menace response is present in most visual birds but may be absent in some eagles that are either normal or that do not have appreciable ophthalmic lesions. Applanation tonometry

and the Schirmer tear test 1 can be performed easily on adult bald eagles and provide reproducible results.

Key words: ophthalmic, tonometry, Schirmer tear test 1, avian, bald eagle, Haliaeetus leucocephalus

Introduction

The bald eagle (Haliaeetus leucocephalus) is among the most recognizable of raptors because of its distinctive appearance and its status as a national symbol. It is also the only eagle unique to North America. Previous to this report, longevity records for bald eagles are 28 years of age in the wild and 36 years of age in captivity. (1) After reaching a critically low number of nesting pairs in 1963, conservation efforts were so successful that the bald eagle was removed from the US Fish and Wildlife Services threatened and endangered species list in 2007. (2) A larger population results in more eagles that require veterinary care, and many debilitated birds are kept in zoos, sanctuaries, and rehabilitation centers. This captive population of bald eagles is aging as husbandry practices improve.

Ophthalmic disease is common in examined raptors, with ocular lesions documented in 14% to 75% of birds. (3-6) The highest prevalence has been documented in wild tawny owls (Strix aluco) with ocular surface lesions present in almost 25% and intraocular lesions present in more than 50% of adult owls. (5) Another study, on a colony of captive screech owls (Megascops asio), reported lesions in 52% of examined eyes, with only 17% of examined birds being free of ophthalmic lesions. (6) The most common ophthalmic abnormalities for these captive owls were eyelid notches, corneal lesions, and lens opacities, and most of these lesions were deemed clinically insignificant. (6) In 2 prospective studies on multiple species of free-living North American raptors, ophthalmic abnormalities were found in 48% (3) and 28% (4) of raptors examined. The most common lesions seen were hyphema, anterior uveitis, vitreal hemorrhage, and retinal detachment secondary to trauma. (3,4) In one of these studies, more than half of the free-living raptors with ocular lesions had abnormalities that were considered to be vision threatening in at least 1 eye. (3)

Lenticular abnormalities have been documented in 12.6% of free-living North American raptors that were presented to a veterinary teaching hospital (3) and 34% of eyes in a colony of captive-born screech owls, with the most severe being hypermature cataracts with associated lens-induced uveitis and iris bombe. (6) In a retrospective study at a wildlife center in Virginia, trauma was by far the most common reason for free-living bald eagle presentations and accounted for 71% of all bald eagle cases. (7) Although captive birds can still experience trauma from events such as collisions with cages, transport, and restraint, the prevalence of severe trauma in captive birds may be less than that for wild animals because injuries from vehicles, weapons, and prey are eliminated. In addition, captive birds are more likely to develop age-related changes because of their lengthened life span.

Vision is considered to be essential for the release of rehabilitated diurnal raptors like the bald eagle because they rely heavily on binocular vision for hunting and flying. (8) However, vision assessment can be difficult because even normal birds can have an inconsistent menace response. (9) Tonometry, pupillary light responses (PLR), and tear production are the most basic ophthalmic diagnostics and are routinely performed on all complete veterinary ocular examinations. However, established normal parameters for the particular species being studied are essential for interpreting these values. Significant differences in intraocular pressure (IOP) between hawks and owls have been documented; therefore, extrapolating normal values among avian species is unreliable. (3,10)

Overall, the diagnosis and management of ophthalmic disease is an important aspect of veterinary care for raptors but is difficult when normal ocular parameters for that species are unknown. Despite the conservation effort to protect the bald eagle and the preponderance of ophthalmic disease in raptors, only a few ophthalmic studies include data from the bald eagle. (10,11) The purpose of this study was to assess normal ocular parameters and describe ophthalmic lesions in a population of captive bald eagles.

Materials and Methods

Sixteen adult captive bald eagles obtained from a raptor rehabilitation, education, and breeding center were examined in this study. They were previously free living but could not be released because of debilitating injuries unrelated to the eyes. All of the birds were maintained as a social group in an outdoor enclosure exposed to the elements and offered a diet that consisted of day-old chicks, coturnix quail (Coturnix japonica), rainbow trout, rats, and mice. Six of the birds were female, and 10 were male. Four birds were considered geriatric; the oldest bird was at least 43 years old, 2 were at least 23 and 20 years of age, and one was at least 19 years of age. The other 12 birds were at least 5 years of age based on head plumage, but a more specific age was unknown because those eagles had been born in the wild and had been in captivity for fewer than 5 years. One geriatric bird had undergone bilateral phacoemulsification without intraocular lens implantation 4.5 years before this study for an immature cataract in the left eye (OS) and a hypermature cataract in the right eye (OD).

The eagles used in the study were examined at the University of Tennessee Veterinary Medical Center (UTVMC). The institutional animal care and use committee of the University of Tennessee approved all procedures. The birds were captured from their enclosure the morning of the examination and transported for approximately 1 hour by van to the UTVMC in large individual carriers. All examinations and diagnostic tests were performed between 10:00 AM and 9:00 PM over the course of 5 days. Each eagle was manually restrained for a complete physical examination, blood collection, and a complete ophthalmic examination. The same 2 examiners (M.J., K.B.) performed physical examinations and blood collection for each bird. The same 2 examiners (S.K., D.H.) performed the ophthalmic examinations on each bird.

All ocular examinations were done in the order described hereafter. The menace response was evaluated bilaterally by waving a hand lateral to the examined eye so as to isolate examination of that eye as much as possible. The hand was kept at least 30 cm from the tested eye to avoid false-positive results due to air currents. A positive response was recorded if the bird consistently turned its head, blinked, or opened its mouth threateningly in response to the menacing gesture. A menace was judged to be inconsistent if the bird moved its head or blinked once but would not do so again with repeated gesturing. A menace was classified as negative if the bird did not blink, move its head, or open its mouth in response to hand motions. A bright, focal, circular light beam from a slit lamp (Kowa SL-15, Kowa, Tokyo, Japan) was used to assess direct and consensual PLRs bilaterally. The Schirmer tear test 1 (STTI) (Intervet Schering Schirmer tear test strips, Box-meer, Netherlands) was done bilaterally in all birds (Fig 1). The distal end of the strip was bent at the notch and placed in the temporal third of the ventral conjunctival fornix of each eye for 60 seconds. The wetted distance along the strip was recorded immediately when the strip was removed from the fornix. A single drop of topical 0.5% proparacaine hydrochloride was then applied to each eye and applanation tonometry (Tonopen Vet, Reichert Inc, Depew, NY, USA) was done. Three tonometric readings with a variance of 5% or less were taken for each eye. Slit lamp biomicroscopy (Kowa SL-15) and indirect ophthalmoscopy (28 D handheld lens, Volk Optical Inc, Mentor, OH, USA; Vantage Plus Wireless Headset, Keeler Instruments Inc, Broomall, PA, USA) were done bilaterally in a darkened room without pharmacologic dilation. Descriptions of lesions were recorded.

[FIGURE 1 OMITTED]

Descriptive statistics were done by computer software (SigmaStat 3.0, Systat Software Inc, San Jos& CA, USA). Tear production and IOP of both eyes (OU) were averaged to give a single value of each parameter of each bird. A paired t test was used to compare values for the left and right eyes. A P value < .05 was considered significant, and power was calculated for insignificant differences.

Results

Results of physical examinations were normal for 2 birds and abnormal for 14 birds. Musculoskeletal abnormalities that prevented release back into the wild were the most common physical findings and were present in 13 birds (81%). One of the birds with a normal physical examination could not be released because of arthritis and historical poor flight ability. The other bird with a normal physical examination had not been released initially due to injuries from gunshot wounds and subsequently was kept in captivity because it was geriatric. Heart murmurs were present in 2 birds (13%). Complete blood cell counts were done for all birds. The only abnormality seen was leukocytosis in 11 birds (69%), and this was attributed to stress from transport.

Complete ophthalmic examinations were done OU for all bald eagles. The menace response was considered normal OU in 13 of 16 birds and abnormal in one eye or OU of 3 birds. Of the 13 birds with normal menace responses OU, 3 birds consistently moved their heads in response to the menace, one moved its head and vocalized when tested, and one opened its mouth threateningly in response to the menace gesture. The remaining 8 birds blinked consistently but did not move their head, vocalize, or open the mouth. One bird lacked a menace response bilaterally and was subjectively noted to be a more docile bird. Two other birds lacked a menace response in 1 eye but had either a normal or inconsistent response in the opposite eye. Direct PLRs were brisk and complete OU in all birds. After the pupil was at its most miotic state, hippus was apparent. This response was slightly variable in duration and intensity among birds. Consensual PLRs were not observed in any eye.

[FIGURE 2 OMITTED]

The mean (SD) tear production was 14 [+ or -] 2 mm/min (range, 8 19 mm/min). The difference in tear production between the OD and OS was not significant (P = .28, power = .99). The mean IOP was 21.5 [+ or -] 1.7 mm Hg (range, 15-26 mm Hg). The difference in IOP between the OD and OS was not significant (P = .86, power = .96).

The normal appearance of the bald eagle eye was characterized (Fig 2). A pale yellow superciliary ridge was present. The globe sat snugly within the orbit and was surrounded by a yellow featherless eyelid margin. Both eyelids rested tightly on the globe, but the lower eyelid was more lax than the upper eyelid. The nictitating membrane originated dorsomedially and swept laterally across the globe. It was translucent and had a network of fine blood vessels across its entirety. The leading marginal pleat of the nictitans was pigmented. The cornea was clear, and either none or a very small margin of sclera was visible. The iris was predominantly a pale yellow with varying degrees of mottled golden to chocolate brown (Fig 3). These darker areas were limited to freckles in some birds or involved a large percentage of the iris in other birds. In the oldest of the examined birds, the iris was diffusely heterogeneously dark brown and golden yellow, with the brown more prominent than in the other birds. Two to 7 pale yellow to dark brown, subtle, incomplete concentric rings were visible on most irides. Pectinate ligaments were visible 360[degrees] at the base of the iris. Just axial to the pectinate ligaments, some birds had focal iris stromal thinning that was apparent as circular defects when examined with the slit beam. The pupil was round. The normal lens was clear, and the nucleus and cortex were easily differentiated on slit lamp biomicroscopy. The fundus was medium brown and homogenous. The pecten was large, dark brown, and pleated, and was located ventrally and slightly temporally. The optic nerve head, which is known to be located beneath the pecten, could not be seen.

At least 1 ocular abnormality was noted in 16 eyes of 10 birds. Of the 10 affected birds, 60% (6/10) had lesions bilaterally, and 40% (4/10) had lesions unilaterally. Three birds had unilateral corneal scars that were of unknown etiology. These scars were circular and superficial, and were located axially, laterally, or ventrolaterally. The aphakic eagle that had undergone phacoemulsification had bilateral linear scars from the clear corneal incisions and bilateral mild posterior capsular opacification. Cataracts were noted in 8 eyes of 5 birds (Fig 4). Bilateral cataracts were noted in 3 birds, and unilateral cataracts were noted in 2 birds. All eyes with cataracts had a normal menace response and were visual. Five eyes had a single incipient anterior subcapsular cataract, 1 eye had an immature anterior subcapsular cataract, and 2 had immature anterior cortical cataracts. Cataracts had been impairing vision in the bird that had undergone bilateral phacoemulsification. The eagle with bilateral immature anterior cortical cataracts was suspected of having visual impairment based on the lenticular involvement and location of the cataracts but still had a normal menace response. Three of the 4 known geriatric birds were or had been affected with bilateral cataracts. Moderate nuclear sclerosis was noted in 2 eyes of 2 birds (12.5%), one of which was known to be geriatric (> 19 years of age). This was not considered to be an abnormality. The age of the other bird with nuclear sclerosis was unknown beyond being older than 5 years.

Indirect ophthalmoscopy was normal OU in 13 of 16 of the eagles (81%). Severe asteroid hyalosis obscured the fundus OD in 1 eagle (Fig 5). This bird lacked a menace response bilaterally, although the only other ophthalmic lesion was a small corneal scar OS, and it was clinically visual. Fundic abnormalities were noted in 3 eyes of 2 birds, all of which were clinically visual. Both of these birds had normal menace responses bilaterally. Chorioretinal scars seen as grayish white, well-demarcated areas of fundic depigmentation were noted bilaterally in 1 bird and unilaterally OD in another bird. These lesions involved 10%, 50%, and 75% of the fundus in the affected eyes, respectively, and varied in location.

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

Discussion

More than half of the eagles in this study had ophthalmic abnormalities, and this is comparable with the previously reported range of 14% to 75% for other raptors. (3-6) Similar to the study in captive screech owls, (6) most of the ophthalmic abnormalities observed in these bald eagles were clinically insignificant at the time of examination. It has been reported that the menace response can be inconsistent in normal birds, which makes vision assessment difficult. (9) Most of the eagles in this study had obvious menace responses indicative of vision. In 1 geriatric bird that lacked a menace response bilaterally, severe unilateral asteroid hyalosis prevented visualization of the fundus OD, which could explain the absent menace response in that eye. However, the menace response was also absent in that bird OS where the only ophthalmic lesion was a small superficial ventrotemporal corneal scar. Furthermore, in 2 other birds with either absent or inconsistent menace responses, no ophthalmic lesions were found that could account for reduced or absent vision. Because they had lived in captivity for several years, the menace response in these birds may have been falsely negative because of habituation to people. Alternatively, the lack of a menace response also may have resulted from extreme fear after being transported and restrained. Less likely, these birds could have had reduced vision in those eyes for unobserved pathologic reasons, such as centrally mediated disease or retinal disease that was not apparent on fundic examination or had not manifested as behavioral changes noted by the keepers. All the birds that had cataracts and chorioretinal scars had normal menace responses bilaterally. Overall, most of bald eagles displayed obvious menace responses with head movement, consistent blinking, and opening of the mouth. However, some bald eagles may not menace despite being free of ocular lesions.

[FIGURE 5 OMITTED]

In contrast to mammals, birds only have a direct PLR. This is because birds, unlike mammals, have complete decussation of the optic nerve fibers at the optic chiasm to the contralateral area pretectalis. (12-14) The posterior commissure then carries the nervous impulse from the contralateral area pretectalis to the ipsilateral Edinger-Westphal nucleus. (13,14) From the Edinger-Westphal nucleus, the signal is transmitted to the ipsilateral ciliary ganglion and iris sphincter muscle. Direct PLRs should be present in birds even though they have voluntary control over pupil size due to the skeletal pupillary sphincter muscle; this muscle results in a more rapid PLR in birds than in mammals. (13) A false-positive consensual PLR can be elicited in some birds when a strong beam of light penetrates through the thin medial orbital bones to stimulate the contralateral retina. (15) This has been previously documented in pigeons (Columba livia) in which the orbits are separated only by a thin membranous septum. (15) However, a consensual PLR could not be elicited in owls. (15) This was attributed to the fact that their nearly parallel visual axis requires positioning the stimulating light in such a way that avoids penetration through the orbital bones. This phenomenon may be similar in bald eagles because none of the examined eagles had consensual PLRs.

Tear production has been evaluated in birds by using both the Schirmer tear test strips and phenol red thread test. (5,6,11,16,17) The STT1 as used in this study measures both basal and reflex tearing. (18) A study by Korbel and Leitenstorfer (11) evaluated tear production via the STT1 for 42 avian species from 7 orders. The highest mean tear production reported in that study was seen in falcons of the subgenus Hierofalco and was 14.4 [+ or -] 7.2 mm/min. Twenty-one birds from 7 species of the order Accipitriformes, including 2 bald eagles, were evaluated. (11) The mean tear production for the order was 11.3 [+ or -] 5.0 mm/min. (11) Mean tear production of the STT1 in Amazon parrots (Amazona ventralis) was 7.9 [+ or -] 2.6 mm/min (range, 0-13 mm/min) (16) and 6.5 [+ or -] 2.9 (range, 1-12 mm/min) in Humboldt penguins (Spheniscus humboldti). (17) In screech owls, median tear production has been reported as [less than or equal to] 2 mm/min (range, [less than or equal to] 2-6 mm/min). (6) We measured mean tear production by using the STT1 at 14 [+ or -] 2 mm/min (range, 8-19 mm/min) in the bald eagle, which is higher than what has previously been reported for most other avian species and similar to that of hierofalcons. This test was easy to perform in the bald eagles, and the lower eyelid mobility in these birds was sufficient to allow placement of the strips. The strips needed to be placed temporally in the ventral cul de sac because the movement of the nictitating membrane pushed the strips out when they were placed centrally.

Tonometry is the indirect measurement of IOP and has been most widely reported by using electronic applanation tonometers. (18) This technique provided reliable IOP measurements on 46 avian species with a minimum corneal diameter of 9 mm. (19,20) Studies that used applanation tonometry have shown that the IOPs of some species of hawks and eagles are not significantly different from each other but are significantly higher than those for owls and kestrels. (3,10) Mean IOP for the bald eagles in this study as measured with applanation tonometry was 21.5 [+ or -] 1.7 mm Hg, with a range of 15-26 mm Hg. This is similar to a previously reported value of mean (SD) 20.6 [+ or -] 2.0 mm Hg from 5 eyes of 3 bald eagles. (10) This value is also similar to reported values for red-tailed hawks (Buteo jamaicensis), Swainson's hawks (Buteo swainsoni), and the golden eagle (Aquila chrysaetos) but higher than what has been reported for owls, American kestrels (Falco sparverius), turkey vultures (Cathartes aura), and Cooper's hawks (Accipiter cooperii). (3,10) Recent studies compared applanation and rebound tonometry in birds of prey. (3,6,21) Rebound tonometry can produce varying IOP values, depending on which calibration curve setting is used, and the resultant IOP may be significantly higher or lower than that measured by applanation tonometry. (6,21) The disparities between applanation and rebound tonometry in raptors are often statistically significant but clinically insignificant. Corneal curvature, eye size, and corneal thickness appear to play a role in raptor tonometry, with rebound tonometry especially being dependent on corneal thickness. (22) Applanation tonometry also has been shown to provide a narrower range of IOP measurements in larger raptors, especially eagles. (22) Significant differences in IOP between juvenile and adult raptors have been found in some species but not in others. (3,23) Because only adult bald eagles were examined in this study, whether or not that difference occurs in bald eagles is still unknown.

Diurnal variations in IOP and tear production have been documented in various species, including birds, humans, dogs, and cats. (24-28) Researching this phenomenon was beyond the scope of this study, but, based on information from other species, diurnal variation would not be likely to alter clinical interpretations of the Schirmer tear test or IOP in the bald eagle. The reported diurnal IOP changes in chickens vary between 4 and 8 mm Hg. (29,30) Pigeons also have a 4 mm Hg diurnal variation in IOP. (30) In the same study, the common buzzard (Buteo buteo) and the tawny owl did not show diurnal variation, although the number of birds evaluated was small. (30) Diurnal tear production fluctuation has not been investigated in raptors but accounts for a difference of less than 3 mm/min in dogs. (24,26,27) Whether or not the bald eagle has diurnal variation in tear production and IOP remains unknown.

The 3 unilateral corneal scars were likely caused by prior trauma. The darkest brown iris was in the most geriatric eagle, which was the bird that had previously undergone bilateral phacoemulsification. Possibilities for this darker iris include a benign aging change, such as stromal thinning, normal variation in iris pigmentation, or iridal hyperpigmentation secondary to chronic lens-induced or postoperative uveitis. However, clinical evidence of uveitis was never observed beyond the immediate postoperative period. In addition, one of us (D.H.) has noted darker irides on aged bald eagles that have not had phacoemulsification.

Cataracts affected 6 birds and threatened vision in 2 birds. One geriatric bird was aphakic bilaterally after phacoemulsification for visually debilitating cataracts. Of the known geriatric birds, 3 of 4 had bilateral cataracts. It is possible that there is an association between age and cataract formation in bald eagles. Ages were unknown in the 3 other birds that had cataracts. Cataracts in raptors are typically attributed to traumatic causes, but age-related cataracts have been reported in an Andean condor (Vultur gryphus) and captive Falconiformes, Sphenisciformes, Galliformes, and Passeriformes. (4,31,32) However, this association in bald eagles is merely speculative because exact ages for the other birds with and without cataracts are unknown. Geriatric cataracts may not be an issue for free-living birds because they may not survive to an age in which cataracts develop or impact vision. Nevertheless, a predisposition for cataract formation in geriatric bald eagles may exist, and this information could be valuable for zoological and rehabilitation centers that care for these aging birds. Three other bald eagles have been seen at the UTVMC for cataracts that were impacting vision to the point of requiring phacoemulsification, and all were known to be at least 20 years of age. These eagles were from the same raptor rehabilitation center but were not included in this study. The incipient anterior cortical cataracts observed in this study possibly will progress with age and result in vision deficits. This would decrease the quality of life and capability of an animal as visually dependent as the bald eagle.

The depigmented fundic lesions were most consistent with inactive chorioretinitis. These lesions could have been caused by prior trauma, which has been documented as the most common cause of ocular lesions in raptors, or infectious disease. (4) The asteroid hyalosis present OD in 1 geriatric bird was likely degenerative and was so dense that it obscured the fundus.

The prevalence of ocular disease in bald eagles is similar to that of other raptors presented to veterinarians and rehabilitation centers. Cataracts may be more prevalent in geriatric bald eagles. Normal bald eagles have direct PLRs but lack a consensual PLR. An obvious positive menace response is present in most visual birds but may be absent in some eagles that are either normal or do not have appreciable ophthalmic lesions. Applanation tonometry and the STT1 can easily be performed on adult bald eagles and provide reproducible results.

Acknowledgments: We thank Misty Bailey for her technical writing support and both the American Eagle Foundation of Pigeon Forge, TN, and Nancy Zagaya for their generosity and cooperation. Financial support was provided by the Companion Animal Fund at the University of Tennessee College of Veterinary Medicine.

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Sonia E. Kuhn, DVM, Michael P. Jones, DVM, Dipl ABVP (Avian), Diane V. H. Hendrix, DVM, Dipl ACVO, Daniel A. Ward, DVM, PhD, Dipl ACVO, and Katherine H. Baine, DVM

From the Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, 2407 River Dr, Knoxville, TN 37996, USA.
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Title Annotation:Original Studies
Author:Kuhn, Sonia E.; Jones, Michael P.; Hendrix, Diane V.H.; Ward, Daniel A.; Baine, Katherine H.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Jun 1, 2013
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