Rehabilitating wild birds of prey following ocular trauma – should foveal assessment include spectral-domain optical coherence tomography?

Abstract

Background

The fovea is an area of increased cone density in the avian retina and provides a high level of visual acuity. Damage to the fovea may negatively impact survival of birds of prey in the wild. The goal of this prospective, descriptive study was to determine whether spectral-domain optical coherence tomography (SD-OCT) imaging results influenced the prognosis for vision prior to release in wild birds of prey following ocular trauma. The birds were manually restrained and underwent a complete ophthalmic examination including SD-OCT imaging. Diagnosis, prognosis for vision, and treatment recommendations were decided twice – immediately following clinical examination, and again following SD-OCT examination. Changes to prognosis and treatment recommendations following SD-OCT examination were noted.

Results

Thirty-seven diurnal and nocturnal wild birds of prey were evaluated. SD-OCT confirmed the prognosis for vision as determined by clinical examination in the majority of cases (22/37), and offered superior lesion evaluation in cases with retinal pathology. In 12/37 birds SD-OCT examination altered the prognosis, leading to a change in treatment recommendation for one bird.

Conclusions

SD-OCT examination provided a detailed, and often superior assessment of foveal anatomy and pathology in awake birds of prey, versus a standard ophthalmic examination with fundus photography alone. Combining ophthalmic examination and SD-OCT findings may allow clinicians to make better informed decisions regarding rehabilitation, and subsequent release of traumatized wild birds of prey, especially if foveal damage is suspected. SD-OCT examination does not seem indicated for birds without ocular abnormalities on ophthalmic examination and fundus photograph evaluation.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12917-025-05245-2.

Background

Predatory birds, including, amongst others, falcons, buzzards, hawks, kites and owls may be collectively referred to as birds of prey [1]. Although grouped under this catch-all term, these birds display many important differences particularly when considering their behaviour, ecology, and certain aspects of their anatomy [2–5]; however, a common thread amongst all birds of prey are their incredible sensory capabilities, in particular vision, which are paramount to their success as predatory species [1, 2, 6].

The avian fundus includes the pecten oculi and the fovea (Fig. 1), two specialized structures which are believed to contribute to the ecology and evolution of both predatory and non-predatory species. The fovea is a cone-rich, rod-free, and typically depressed/invaginated area within the neurosensory retina, providing exquisitely high spatial resolution in avian species [1, 6–8]. The fovea imparts colour vision, depth perception, and provides the highest visual acuity, thus representing a critical structure for predatory wild birds of prey [6, 8–10]. Foveae differ greatly among different species, including their structure and number [1, 6, 9, 11]. Certain diurnal birds of prey including falcons, hawks, buzzards and eagles are bifoveate, possessing both a central and temporal fovea, whereas owls and most other birds possess a single temporal fovea only [1, 6]. The central fovea is typically of a deep and convexiclivate nature, whereas the temporal fovea in bifoveate birds of prey and in owls tends to be shallower or even of the fovea plana type [1, 3, 6] (Fig. 2). The temporal foveae are required for the fixation of near objects and for stereopsis, whereas fixation of distant objects is the task of the central fovea [1, 2, 6, 11]. The number and location of foveae is generally accepted to be secondary to the type of hunting/predation behaviour the species in question engages in, their environment, and the evolution of their anatomy.

Fig. 1.

Representative fundus photograph and SD-OCT B-scan image of an unaffected common buzzard. A. Fundus photograph indicating the pecten and the temporal (TF) and central (CF) convexiclivate foveae of a common buzzard (Buteo buteo). B. SD-OCT image illustrating both foveae and the retinal layering as visible on OCT. NFL = nerve fiber layer; GCL = ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer; ELM = external limiting membrane; MZ = myoid zone; EZ = ellipsoid zone; PROS/IZ = combination of photoreceptor outer segments and interdigitation zone with RPE; RPE/BM = retinal pigment epithelium/Bruch’s membrane complex; CC = choriocapillaris; SD-OCT = spectral-domain optical coherence tomography

Fig. 2.

Representative SD-OCT B-scan images of the three different conformations of foveae observed in birds of prey enrolled in this study. A. Common buzzard (Buteo buteo): diurnal bifoveate bird of prey with central and temporal convexiclivate foveae. B. Red kite (Milvus milvus): diurnal bifoveate bird of prey with central convexiclivate fovea and temporal fovea plana. This image is a composite of two OCT B-scan images. C. Tawny owl (Strix aluco): nocturnal bird of prey with a single temporal fovea. CF = central fovea; TF = temporal fovea; SD-OCT = spectral-domain optical coherence tomography

The pecten oculi is a highly vascular structure, interwoven with pigmented tissue overlying the optic nerve head [8]. Of the three reported types, the pleated type is found in most birds, and has been most extensively studied [8, 12, 13]. Numerous potential functions of the pecten oculi have been proposed. That it provides blood and therefore nutrition to the anangiotic avian retina is the most widely accepted function [8, 13]; however, it has also been suggested to engage in other functions including providing protection from UV light [13]. Although the precise function(s) of the pecten remains somewhat of a mystery, it is widely accepted that a functional pecten is critical to the health and function of the avian retina, and damage to this structure may result in reduced retinal function, and therefore a decrease in vision. As wild birds of prey are reliant on their sensory capabilities to hunt prey successfully, any hindrance to these abilities would have significant negative connotations for the ability of the affected bird to hunt, and thus survive, in the wild.

Wild birds of prey are particularly susceptible to trauma due to the impact of humans on their habitat, and the propensity of some types of bird of prey to feed on carrion, often roadkill in urban and suburban areas, increasing their chances of being struck by a vehicle [14, 15]. Numerous types of bird of prey are considered protected or endangered species, and conservation efforts of these avian species should be a priority [14]. Reductions in bird of prey populations may have a far-reaching impact not only on genetic diversity, but also for maintaining the ecology and balance of natural environments [14]. In addition, many rehabilitation centers often operate under very tight financial constraints, and investment into rehabilitating a bird with a poor chance of success in the wild would be a poor use of resources. It is therefore critical to invest in individuals where the chances for successful release into the wild may be maximized [16]. A number of authors have proposed the weighing of various release criteria for birds of prey following trauma, including lesion extension, location, chronicity, laterality, systemic health and body condition, flight and prey catching behaviour in a flight cage, and species, type and age [1, 17–21]. General consensus exists regarding the importance of foveal health as release criterium.

Optical coherence tomography (OCT) is a non-invasive imaging technique which produces a two-dimensional image of biological tissues using their optical scatter [22–25], and provides an image resolution akin to low-power histology [24]. Spectral domain OCT (SD-OCT) is a modification which enables high-speed scanning and improved image resolution, and due to the transparency of many ocular structures, imaging of both the anterior and posterior segment is possible [8, 26, 27]. The use of OCT/SD-OCT is well established in both human and veterinary medicine for the evaluation of retinal diseases, including those of traumatic origin where some clarity of the ocular media is maintained, and represents an effective modality to image the retina and foveae [7, 8, 28–30].

To the authors’ knowledge, there is no published study specifically evaluating SD-OCT findings in birds of prey following trauma, or the impact of SD-OCT findings on prognosis in affected birds especially as this relates to foveal health. The purpose of this study was therefore to determine whether SD-OCT findings influence the prognosis for foveal health, as a surrogate for vision assessment in wild birds of prey following trauma.

Methods

Wild birds of prey presented due to suspected trauma to the Animal Hospital of the Vetsuisse Faculty at the University of Zurich in Switzerland between 2017 and 2023 were included in this prospective, descriptive study. Birds underwent a complete ophthalmic examination by a board certified veterinary ophthalmology diplomate and/or resident, including neuro-ophthalmic examination, tonometry (Tonovet^® Type TV01, Icare, Tiolat Oy, Finland), slit-lamp biomicroscopy (Kowa SL-17 portable slit-lamp, Kowa Company Ltd, Tokyo, Japan), fluorescein stain (Fluo^® strips, Contacare Ophthalmics and Diagnostics, Gujarat, India) and binocular indirect ophthalmoscopy (mPack Unplugged, Heine, Germany) using a 28D indirect ophthalmoscopy lens (Volk^® 28D bio lens, Ohio, USA). Wherever possible, fundus photography was performed (Optomed Smartscope MS, Optomed Oy, Oulu, Finland 2017–2022 or Optomed Aurora Retinal Module, Optomed Oy, Oulu, Finland 2022–2023) to complement examination findings. Spectral-domain optical coherence tomography examination was performed immediately following ophthalmic examination. All birds were manually restrained in an upright position without the use of sedation or general anesthesia (Fig. 3). A commercially available, table-mounted, high-resolution SD-OCT instrument with an axial pixel resolution of 2.4 μm (Bioptigen Envisu R2210 SD-OCT; Leica Microsystems, Wetzlar, Germany) equipped with a General Retina lens (Bioptigen Envisu) was used to image the fundus in all birds. Room lights and SD-OCT instrument search lights were switched off to maximize pupil diameter. The General Retina lens was set to -2 Diopters, and the SD-OCT reference arm length varied between 340 and 390 depending on anteroposterior globe diameter. To obtain cross-sectional images through the central retina, including the pecten/optic nerve head and foveal regions, horizontal volume scans (6 × 6, 8 × 8, or 10 × 10 mm depending on the region of interest, 100 B-scans per volume scan and 1000 A-scans per B-scan) were obtained. Attempts were made to align the central and temporal fovea in bifoveate species. Birds with and without signs of ocular pathology were included if the ophthalmic examination could be completed, and if the SD-OCT examination yielded images of diagnostic quality for at least one eye. Diagnostic quality images were defined as volume scans included of pecten, foveal region(s) and central retina, with sufficient contrast and definition to clearly distinguish the retinal and subretinal layers within the scan range (subjective assessments, all performed by one examiner (SAP)). Birds with eyes in which the fundus was partially obscured by more anteriorly located pathologies were also included. Immediately following ophthalmic examination, a standardized score sheet was completed based on ophthalmic examination findings using a modified McDonald-Shadduck scoring system to grade changes in the anterior and posterior segments [31] (Supplementary Fig. 1 and description scoring system). Subsequently, an SD-OCT examination was performed, a second score sheet was completed, and the prognosis for vision was again determined, this time based on the combination of ophthalmic examination and SD-OCT findings. The final prognosis for vision was determined based on the prognosis for the worst of the two eyes examined, according to a standardized prognosis scoring sheet (Supplementary Fig. 2), and was utilized to determine the overall prognosis for vision for every patient. Findings from the complete ocular examination as well as the systemic status of the bird were then discussed with the attending clinician of the Clinic for Zoo Animals, Exotic Pets and Wildlife, leading to an overall patient prognosis and recommendations for the most appropriate course of action for every bird, including rehabilitation (treatment and reassessment, if indicated), release, or euthanasia. In select cases, a recheck ophthalmic examination, including SD-OCT, was performed following appropriate systemic therapy, as determined by veterinarians from the Clinic for Zoo Animals, Exotic Pets and Wildlife. In these cases, prognosis was determined again following re-evaluation. In cases where euthanasia was performed, birds were sedated with a combination of 50 mg/kg of ketamine (Ketnarkon 100, Streuli Pharma AG, Uznach) and 0.5 mg/kg of medetomidine (Medetor^®, Virbac) via intramuscular injection, followed by 1 mg/kg of pentobarbital (Esconarkon^®, Streuli Pharma A, Uznach) via intravenous or intracardiac injection, based on bird size and clinician preference.

Fig. 3.

Birds were gently manually restrained for ophthalmic and SD-OCT examinations. A. Common buzzard (Buteo buteo) being wrapped in a towel for gentle restraint during the examination. B. Common buzzard placed on a towel pad in front of the SD-OCT scan lens. SD-OCT = spectral-domain optical coherence tomography

Descriptive statistics were performed on the collected data using Microsoft Excel™.

Results

Examinations were performed on 37 wild birds of prey, encompassing 10 different species, including diurnal and nocturnal species (Table 1). No examination-induced adverse effects were noted during any of the ophthalmic or SD-OCT examinations for any of the birds.

Table 1.

Patient demographics of 37 birds of prey. Chronological, not alphabetical:

	Latin Name	Species	Type	Weight	Sex	Eye(s)
1	Buteo buteo	Common buzzard	Diurnal	?	?	OU
2	Buteo buteo	Common buzzard	Diurnal	875 g	M	OD
3	Buteo buteo	Common buzzard	Diurnal	515 g	M	OD
4	Falco tinnunculus	Common kestrel	Diurnal	150 g	F	OD
5	Milvus milvus	Red kite	Diurnal	864 g	?	OD
6	Accipiter nisus	Eurasian sparrowhawk	Diurnal	230 g	F	OD
7	Strix aluco	Tawny owl	Nocturnal/some diurnal activity	440 g	?	OU
8	Pandion haliaetus	Osprey	Diurnal	1.73 kg	?	OS
9	Accipiter gentilis	Northern goshawk	Diurnal	?	?	OD
10	Accipiter nisus	Eurasian sparrowhawk	Diurnal	?	?	n/a
11	Buteo buteo	Common buzzard	Diurnal	655 g	?	n/a
12	Milvus milvus	Red kite	Diurnal	857 g	?	n/a
13	Buteo buteo	Common buzzard	Diurnal	640 g	M	OS
14	Strix aluco	Tawny owl	Nocturnal/some diurnal activity	595 g	F	OU
15	Buteo buteo	Common buzzard	Diurnal	870 g	?	OD
16	Asio otus	Long eared owl	Nocturnal	265 g	?	OU
17	Strix aluco	Tawny owl	Nocturnal/some diurnal activity	490 g	?	OS
18	Buteo buteo	Common buzzard	Diurnal	625 g	M	OU
19	Falco subbuteo	Eurasian hobby	Diurnal	178 g	?	n/a
20	Buteo buteo	Common buzzard	Diurnal	690 g	?	n/a
21	Buteo buteo	Common buzzard	Diurnal	575 g	?	n/a
22	Milvus migrans	Black kite	Diurnal	780 g	?	OU
23	Buteo buteo	Common buzzard	Diurnal	800 g	?	OU
24	Asio otus	Long eared owl	Nocturnal	?	?	OD
25	Accipiter gentilis	Northern goshawk	Diurnal	620 g	M	n/a
25	Milvus milvus	Red kite	Diurnal	860 g	?	n/a
27	Falco tinnunculus	Common kestrel	Diurnal	180 g	?	OS
28	Falco tinnunculus	Common kestrel	Diurnal	180 g	F	OU
29	Buteo buteo	Common buzzard	Diurnal	?	?	OD
30	Milvus milvus	Red kite	Diurnal	980 g	?	OD
31	Buteo buteo	Common buzzard	Diurnal	960 g	?	OU
32	Buteo buteo	Common buzzard	Diurnal	875 g	F	OU
33	Falco subbuteo	Eurasian hobby	Diurnal	280 g	F	OU
34	Falco tinnunculus	Common kestrel	Diurnal	140 g	M	n/a
35	Buteo buteo	Common buzzard	Diurnal	574 g	?	OU
36	Falco tinnunculus	Common kestrel	Diurnal	170 g	F	OS
37	Milvus milvus	Red kite	Diurnal	783 g	?	OU

Legend: M = male, F = female, Eye = affected eye, OD = right eye, OS = left eye, OU = both eyes, n/a = not affected, ? = unknown

Included in the study are results from 14 common buzzards (Buteo buteo), five each of the common kestrel (Falco tinnunculus) and red kite (Milvus milvus), three tawny owls (Strix aluco), two each of the northern goshawk (Accipiter gentilis), Eurasian sparrowhawk (Accipiter nisus), long eared owl (Asio otus), and Eurasian hobby (Falco subbuteo), and one each of the black kite (Milvus migrans) and osprey (Pandion haliaetus) (Table 1, Supplementary Table 1). A total of seven female and six male birds and 24 birds of unknown sex are included. The weight range of all birds included was 140 g (common kestrel) to 1.73 kg (osprey). Patient demographics are summarized in Table 1.

Based on the clinical examination the right eye (oculus dexter, OD) was affected in 10 birds, the left eye (oculus sinister, OS) was affected in five birds, both eyes (oculus uterque, OU) were affected in 13 birds, and both eyes were unaffected in nine birds. The anterior segment was affected in 19 birds (20 eyes), the posterior segment was affected in 19 birds (27 eyes), and both eyes were unaffected in nine birds (18 eyes) for a total of 37 birds (74 eyes) (Table 1, Supplementary Table 2). The most common clinical examination diagnoses for the anterior segment included uveitis (eight eyes), angle recession (five eyes), lens subluxation/luxation (four eyes), hyphema (three eyes) and cataract formation (three eyes) (Supplementary Table 2, Fig. 4). The most common clinical examination diagnoses for the posterior segment included vitreal hemorrhage (18 eyes), retinal degeneration (nine eyes) and retinal detachment (three eyes) (Supplementary Table 2, Figs. 5 and 6). Eight examined eyes were assessed to be blind. Results for clinical examination diagnoses are summarized in Supplementary Table 2.

Fig. 4.

Anterior segment lesions as observed in study patients. A. Long eared owl (Asio otus) with keratic precipitates and mild hyphema OS. B. Eurasian sparrowhawk (Accipiter nisus) with temporal angle recession, lens subluxation and a cataract OS. C. Red kite (Milvus milvus) with nasal angle recession and chronic uveitis that resulted in posterior synechiae and pigment deposition on the anterior lens capsule OS. OS = oculus sinister

Fig. 5.

Fundus photographs and SD-OCT B-scan images of a tawny owl at initial and two-week recheck examinations. A. Fundus photograph of the central fundus OD of a tawny owl (Strix aluco) demonstrating loss of fundus definition nasal to and surrounding the tip of the pecten, with subtle discolouration of the fundus temporal to and surrounding the tip of the pecten. B, C. SD-OCT B-scan images demonstrating: mild irregularities in outer retinal thickness (distance ELM-RPE/BM) and reflectivity, a hyper-reflective signal throughout the retinal layers and some loss of definition of the ELM and EZ towards the right side of the scan; the fovea appears unaffected (B); and small areas of retinal detachment adjacent to the pecten, associated with a hyper-reflective signal throughout the overlying retinal layers, and local disruption of the ELM, EZ, and the rest of the outer retina (C). D. Two-week recheck fundus photograph demonstrating patchy pigment irregularities and overt depigmentation and hyperpigmentation. The pecten appeared unaffected. E, F, G. The recheck SD-OCT B-scan images demonstrate disruption of all retinal layers between and including the OPL and RPE/Bruch’s membrane complex, with damage mostly restricted to the photoreceptors in the outer retina (E, F) as typical traumatic ‘contrecoup’ damage to photoreceptor inner and outer segments (comparable to commotio retinae in human patients). The fovea remained unaffected, as illustrated on OCT scan F. OCT scan G illustrated a persistent hyper-reflective signal affecting the inner retinal layers and complete disruption of outer retinal architecture immediately adjacent to the pecten, indicative of predominantly outer retinal degeneration following previous retinal detachment (C). The bird was sent to the rehabilitation facility as significant portions of the retina were preserved and the fovea was unaffected at the two-week recheck examination.The green lines in the fundus photographs A and D represent the scan lines of the horizontal OCT B-scan images B, C, E, F and G. OD = oculus dexter; ELM = external limiting membrane; EZ = ellipsoid zone; OPL = outer plexiform layer; SD-OCT = spectral-domain optical coherence tomography

Fig. 6.

Fundus photographs and SD-OCT B-scan images of a common buzzard, red kite and tawny owl at initial examination. A. Fundus photograph of the central fundus OD of a common buzzard (Buteo buteo) demonstrating patchy pigment irregularities, depigmentation and hyperpigmentation surrounding the temporal fovea. The central fovea and pecten seemed unaffected. B, C, D. The SD-OCT B-scan images demonstrated disruption of all retinal layers between and including the ELM and RPE/Bruch’s membrane complex around the temporal fovea (damage was mostly restricted to the outer retina). The temporal fovea showed focal disruption of the ELM, EZ and RPE/Bruch’s membrane complex (B). Scan C demonstrated focal reflection irregularities in the PR inner and outer segment region adjacent to a temporal region of full thickness retinal degeneration. Scan D demonstrated PR inner and outer segment reflection irregularities in the center of the central fovea. The bird was euthanized due to a suspicion of blindness OD based on its flight behaviour in the rehabilitation center, and due to the right central and temporal foveal changes observed on OCT. E. Fundus photograph of the central fundus OD of a red kite (Milvus milvus) demonstrating a well demarcated area of depigmentation, pigment irregularities, and patchy fundus discoloration in the immediate vicinity of the temporal fovea. The central fovea and pecten seemed unaffected. F, G. The SD-OCT B-scan images demonstrated complete disruption of all PR layers and hyper-reflectivity of and loss of definition between NFL, GCL and IPL immediately temporal to the temporal fovea (F). The central fovea was unaffected (G). As it was clinically unremarkable, this bird was released into the wild. H, I. Fundus photograph and SD-OCT scan volume intensity projection of the central fundus OS of a tawny owl (Strix aluco) demonstrating vitreal hemorrhages, seen as fine irregularly shaped red lines nasal to the pecten on the fundus photograph (H), and as irregularly shaped black fine lines and masses surrounding the pecten, predominantly on the nasal side (I). The pecten seemed unaffected. J. The SD-OCT B-scan image demonstrated multiple vertical linear shadows caused by small vitreal hemorrhages. The bird was sent to the rehabilitation facility since the retinal architecture, pecten, optic nerve and fovea were unaffected. The green lines in the fundus photographs A and E, and volume intensity projection I represent the scan lines of the horizontal OCT B-scan images B, C, D, F, G and J. CF = central fovea; TF = temporal fovea. OS = oculus sinister; OD = oculus dexter; SD-OCT = spectral-domain optical coherence tomography; ELM = external limiting membrane; EZ = ellipsoid zone; PR = photoreceptor; NFL = nerve fiber layer; IPL = inner plexiform layer; GCL = ganglion cell layer

The SD-OCT examinations for 34/37 birds were performed by the same examiner (SAP), with 3/37 birds evaluated by a different examiner (AL). The most common SD-OCT diagnoses/findings included photoreceptor layer damage (11 eyes), vitreal hemorrhage (nine eyes), foveal damage (seven eyes), retinal degeneration (six eyes), and retinal detachment (five eyes) (Figs. 5 and 6). The fundus was impossible to evaluate partially or completely in five eyes due to anterior or posterior segment pathologies; Supplementary Table 2 summarizes the SD-OCT findings/diagnoses. Recheck examinations were performed in nine birds (# 5, 7, 14, 17, 27, 31, 32, 33, 34), including six birds (# 5, 7, 27, 31, 32, 33) that underwent repeat SD-OCT examinations, with one bird (# 31) undergoing two recheck SD-OCT examinations. Repeat SD-OCT examinations were performed specifically due to concerns related to foveal health. The foveae could be evaluated in detail in four of these six birds at the recheck examinations, and despite the presence of retinal degeneration in some birds, the foveae appeared unaffected on SD-OCT. In one bird (# 31), the initial recheck examination performed approximately two weeks after the baseline exam revealed full thickness damage of the central fovea OD, with potential damage to the central fovea OS found on the second recheck OCT examination approximately six weeks later. These findings resulted in euthanasia due to a poor prognosis for vision. In the last of these six birds (#32), remaining organized vitreal hemorrhage prevented OCT evaluation of the temporal fovea OD. Since no lesions were observed OS, or in the visible portions of the retina and central fovea OD, damage to the temporal fovea OD was deemed unlikely, and the bird was sent to the rehabilitation facility (Supplementary Table 2, Table 2).

Table 2.

Foveal involvement, prognosis, plan and outcome for 37 birds of prey

Patient #/species	Px change d/t OCT	Overall Px for vision	Plan change d/t OCT	Foveal involvement	Outcome
1 Common buzzard	N	Fair	N	N	Rehab → released
2 Common buzzard	N	Poor	N	Y (OD)	Euthanasia d/t blindness OD in rehab center
3 Common buzzard	N	Guarded	N	?	Euthanasia d/t poor prognosis for vision
4 Common kestrel	N	Guarded	N	?	Rehab → euthanized
5 Red kite	N	Fair	N	N	Released
6 Eurasian sparrowhawk	N	Poor	N	Y (OD)	Euthanasia d/t blindness OD
7 Tawny owl	Y	Fair	N	N	Rehab → released
8 Osprey	Y	Excellent	N	N	Euthanasia d/t humeral fracture
9 Northern goshawk	N	Excellent	N	N	Rehab → released
10 Eurasian sparrowhawk	N	Excellent	N	N	Rehab → released
11 Common buzzard	N	Excellent	N	N	Rehab → released
12 Red kite	N	Excellent	N	N	Rehab → released
13 Common buzzard	N/A	Poor	N	?	Rehab → euthanized
14 Tawny owl	Y	Poor	N	N	Rehab → released
15 Common buzzard	N	Poor	N	?	Euthanasia d/t poor systemic status and prognosis for vision
16 Long eared owl	Y	Good	N	N	Rehab → released
17 Tawny owl	N/A	Poor	N	?	Euthanasia d/t poor systemic status and prognosis for vision
18 Common buzzard	Y	Guarded	N	?	Euthanasia d/t blindness
19 Eurasian hobby	N	Excellent	N	N	Rehab → released
20 Common buzzard	Y	Good	N	N	Euthanasia d/t poor systemic status
21 Common buzzard	N	Excellent	N	N	Rehab → released
22 Black kite	N	Excellent	N	N	Rehab → released
23 Common buzzard	Y	Fair	N	?	Euthanasia d/t humeral fracture
24 Long eared owl	N	Poor	N	Y (OD)	Rehab → released
25 Northern goshawk	N	Excellent	N	N	Rehab → released
26 Red kite	N	Excellent	N	N	Rehab → released
27 Common kestrel	Y	Good	N	N	Rehab → released
28 Common kestrel	Y	Poor	N	?	Euthanasia d/t humeral fracture and blindness OD
29 Common buzzard	N/A	Poor	N	?	Euthanasia d/t blindness OD
30 Red kite	N	Good	N	N	Released
31 Common buzzard	Y	Poor	Y	Y (OU)	Euthanasia d/t poor prognosis for vision
32 Common buzzard	Y	Fair	N	?	Rehab → released
33 Eurasian hobby	Y	Good	N	N	Rehab → released
34 Common kestrel	N	Excellent	N	N	Rehab → released
35 Common buzzard	N	Poor	N	Y (OS)	Euthanasia d/t blindness OS
36 Common kestrel	N	Poor	N	Y (OS)	Euthanasia d/t blindness OS
37 Red kite	N	Good	N	N	Released
Total	Y = 12		Y = 1	Y = 6, ? = 10	Release = 21, Euthanasia = 16

Legend: Px = prognosis (refers to prognosis for the bird as a whole, as determined by the most severely affected eye if OU affected), d/t = due to, OCT = optical coherence tomography, Y = yes, N = no, ? = unknown, N/A = not applicable, OD = oculus dexter, OS = oculus sinister

Twenty-one of the birds evaluated appeared to have no foveal involvement as determined on SD-OCT examination, foveal involvement was identified in six birds, and foveal involvement was unknown/questionable in ten birds. A total of 14 birds were euthanized, three were released within days of examination, and 20 entered the rehabilitation facility.

Of the 14 birds that were euthanized, eight were euthanized due to blindness or poor prognosis for vision, three were euthanized due to a combination of blindness/poor prognosis for vision and systemic co-morbidities (e.g., orthopedic injuries) and three birds were euthanized due to systemic co-morbidities (two due to humeral fractures) despite a fair to excellent overall prognosis for vision. Five of six birds with confirmed foveal involvement were euthanized due to blindness or poor prognosis for vision. The sixth bird with confirmed foveal involvement entered the rehabilitation facility. Of the 10 birds with questionable foveal involvement, three were euthanized due to blindness or poor prognosis for vision, three were euthanized due to a combination of blindness/poor prognosis for vision and systemic co-morbidities, one was euthanized due to a humeral fracture, and three entered the rehabilitation facility. Results for foveal involvement and overall outcome are presented in Table 2. Overall, 12 of 16 birds with confirmed or questionable foveal involvement were euthanized, compared to two of 21 birds with unaffected foveae.

Of the 21 birds in which the SD-OCT examination confirmed the absence of foveal involvement, 12 had no trauma-relevant ocular changes identified on initial clinical examination, including the evaluation of fundus photographs. In the nine birds that did demonstrate trauma-relevant ocular changes on clinical examination, the SD-OCT examination revealed a normal fundus in three birds, focal photoreceptor inner and outer segment changes in four birds, and focal/multifocal retinal degeneration in two birds, combined with a focal retinal detachment in one of these two.

Of the 12 birds that had no trauma-relevant ocular abnormalities identified on initial clinical examination (one case each with incipient anterior cortical cataracts, focal corneal subepithelial opacities, and focal corneal epithelial opacities), only one bird (#20) demonstrated multifocal photoreceptor inner and outer segment opacities not involving the foveae on OCT. This was the only bird in this group of 12 that was euthanized, but based on its poor systemic health status as the SD-OCT findings were deemed too subtle to negatively affect visual rehabilitation.

In 12 of 37 birds, the SD-OCT examination resulted in an alteration of the overall prognosis for vision. However, in 11 of these 12 birds the treatment recommendation did not change as a result of the SD-OCT examination-based visual prognosis change. In four of these 11 birds (all euthanized) the treatment recommendation was driven by non-ocular (e.g. systemic, orthopedic) findings, and in six of these 11 birds (5/6 sent to rehabilitation) the change in overall prognosis for vision changed insufficiently to alter the treatment recommendation. Only in bird #31 did the change in prognosis lead to an alteration of the clinical recommendations and treatment plan, resulting in euthanasia with identification of bilateral foveal involvement resulting in poor prognosis for vision. Twenty birds were sent to the rehabilitation facility, and of these, 18 were released. The remaining two birds were unilaterally blind diurnal birds of prey, both of which were euthanized due to poor flight cage performance.

Discussion

The purpose of this study was to explore the utility of SD-OCT as a surrogate for vision assessment in birds of prey following suspected trauma. These species of birds appear particularly prone to trauma [14, 15, 32] with potentially devastating sequelae including orthopedic, internal, central nervous system and ophthalmic injuries [32]. A recent study hypothesized that one reason that birds of prey are predisposed to injuries secondary to motor vehicular trauma is due to their propensity to scavenge carrion, in particular, roadkill [15]. A subsequent study from 2022 noted that the second most common cause for morbidity/mortality for vulture species was traumatic injury [14]. Trauma was the main cause for admission of wild birds of prey to rehabilitation centers, with an incidence of 22–70%, depending on the study [33–36], and the reported prevalence of ocular lesions in birds of prey presented to rehabilitation facilities or veterinary clinics ranges from 7–75% [1],[19],[33],[37],[38],[39]. In the present study, ocular changes were identified on clinical examination in 28 of 37 birds (76%), and 39 of 74 eyes (53%), with posterior segment changes being more common than anterior segment changes. The wide variation in reported ocular lesions is likely due to multiple factors, including whether or not all birds in the aforementioned studies underwent a comprehensive ophthalmological examination, the experience level/expertise of the individual performing the examination, whether or not specialized equipment was utilized for the examination, and whether fundus evaluation included photography, ultrasound examination, electroretinography (ERG) and/or SD-OCT. This study demonstrated that SD-OCT examination can provide convincing proof of foveal involvement or non-involvement in the majority of cases (Table 2), and collectively, these studies emphasize the importance of performing a comprehensive ophthalmic examination in all birds of prey following suspected trauma, in addition to determining overall systemic health status.

Birds of prey with bilateral blindness or severe vision impairment are generally considered unfit for release into the wild. For example, in a 2022 study evaluating wild owl species with chorioretinal lesions suspected due to blunt ocular trauma using OCT, all patients were euthanized due to a poor prognosis with the majority of owls being bilaterally affected [40]. Whether birds of prey with unilateral blindness or unilateral severe vision impairment can be released depends on a number of factors and is not generally agreed upon. The release of owls with unilateral blindness or vision impairment has found some acceptance since owls are considered to be less dependent on vision alone for successful prey capture, and some evidence for the successful release of unilaterally visually-impaired owls exists [1, 20, 41]. Diurnal birds of prey with significant unilateral vision impairment are generally not released, with some exceptions made for recently found adult birds with chronic ocular changes and in good body condition [1, 17, 20, 21, 41]. In the present study, the only two birds which were euthanized in the rehabilitation facility were the unilaterally blind diurnal birds of prey, as both displayed poor flight cage performance and hunting abilities. In contrast, two unilaterally blind owls were noted to display successful hunting behaviour in the rehabilitation facility, and were subsequently released, findings which may support the previously held belief that unilaterally blind nocturnal birds of prey may still be effective hunters [1, 20, 41].

In the study presented here, the prognosis for affected birds was determined following ophthalmic examination and again following SD-OCT examination. Although the SD-OCT examination resulted in an alteration of the overall prognosis for vision in 12 of 37 birds in the present study, this change in prognosis led to an alteration of the clinical recommendations and treatment plan in one bird only with bilateral foveal involvement. Blindness and/or confirmed or questionable involvement of the foveae led to a poor overall prognosis for vision and the recommendation for euthanasia in the majority of cases (Table 2). Fourteen of 16 birds which were euthanized had questionable or confirmed foveal pathology based on the clinical ophthalmic and SD-OCT examinations, and 13 of these 16 birds were blind and/or were considered to have a poor overall prognosis for vision in one or both eyes. Furthermore, 15 of 16 birds that were euthanized were diurnal birds of prey, with one owl being euthanized due to a combination of poor systemic health status and poor prognosis for vision. Overall, 14 of 16 birds with confirmed or questionable foveal involvement were euthanized, compared to two of 21 birds with unaffected foveae.

The authors acknowledge that SD-OCT is not a modality that is available to all ophthalmologists or practicing wildlife veterinarians, with most available SD-OCT units being found at universities. This poses an accessibility challenge for many wildlife rehabilitation centers, unless they are near a university where SD-OCT is available, or there is an active wildlife service operating out of the same facility. The equipment itself is not inexpensive, typically costing tens of thousands of dollars, and advanced knowledge of ocular anatomy would be considered a pre-requisite for interpreting the images acquired. However, in the authors’ experience, most trained ophthalmologists would be able to acquire the skills to obtain diagnostic quality images relatively quickly, should the modality be available to them.

Currently, the authors’ routine approach for a pre-release evaluation of a wild bird of prey with trauma history includes an ophthalmic examination and fundus photograph evaluation. Due to a lack of contrast in the avian fundus, it can be very challenging to distinguish the foveae from their surroundings using indirect ophthalmoscopy alone, and fundus photography provides a significant aid in visualization and evaluation of the foveae. The recommendation to perform an SD-OCT examination at our institution is now based on a suspicion of foveal involvement raised when observing fundus abnormalities in the vicinity of the foveae, or not being able to identify/visualize the foveae on indirect ophthalmoscopy or fundus photographs. As demonstrated in this study, SD-OCT is a non-invasive examination [25] which can be readily performed to acquire diagnostic images in awake birds of prey. This finding is clinically relevant as many of these birds were presented following a suspected or known traumatic event, where sedation or general anesthesia may have posed a risk to their systemic status. However, only one of 12 birds that had no trauma-relevant ocular abnormalities identified on initial clinical examination, including fundus photograph evaluation, demonstrated any retinal changes on SD-OCT, which were mild and did not involve the foveae. Although the SD-OCT examination does not seem to be specifically indicated for this cohort of birds, the authors contend that as the field of veterinary ophthalmology continues to advance, it will become more mainstay and may be very clinically relevant in select cases involving threatened or endangered species.

Limitations of the present study include the inability to perform a comprehensive SD-OCT examination in cases of anterior or posterior segment opacities, which consisted of vitreal hemorrhages in the majority of cases. Additionally, evaluation of retinal function using ERG could have been considered as a complimentary test to SD-OCT and complete ophthalmic examination. However, ERG findings may not accurately predict foveal function, and a previous study utilizing ERG in birds of prey noted that this test cannot be used in lieu of imaging and complete ophthalmic examination [19]. Ocular ultrasound could also have been considered in birds where the ocular media was opaque; however, due to the “noncontact” nature of the study, and to limit stress on the birds, especially as ultrasound would be unlikely to identify retinal degeneration or contrecoup injuries, this imaging modality was not utilized. The number of birds undergoing recheck examinations was also small (nine clinical, six clinical + SD-OCT). These were predominantly birds with widespread vitreal hemorrhages (6) or hyphema (2) precluding assessment of the presence and magnitude of foveal involvement. Lastly, given the initial learning curve associated with performing SD-OCT examinations, it is possible that subtle findings associated with retinal changes may have been missed during earlier examinations even though all SD-OCT scans were reviewed during the data analysis phase of the study.

Conclusions

Spectral-domain optical coherence tomography is a non-invasive imaging modality which can be performed in awake birds of prey with results that are of diagnostic quality. The use of SD-OCT imaging as part of the pre-release evaluation of wild birds of prey with a history of trauma resulted in an alteration of the overall prognosis for vision in one third of the examined birds in the present study, but was significant enough to lead to an alteration of the clinical recommendation in one bird only. Spectral-domain optical coherence tomography examinations provided convincing proof of foveal involvement or non-involvement in the majority of cases, and should therefore be considered if results from a comprehensive ophthalmic examination are prognostically inconclusive, especially when foveal involvement is suspected. However, SD-OCT examination does not seem to be indicated for birds that do not demonstrate trauma-relevant ocular abnormalities on ophthalmic examination and fundus photograph evaluation. Future studies should further evaluate the usefulness of performing recheck SD-OCT examinations, and include the final outcome for birds sent to rehabilitation facilities, and following release into the wild.

Abbreviations

IOP

Intraocular pressure

n/a

Not applicable

OD

Oculus dexter, right eye

OS

Oculus sinister, left eye

OU

Oculus uterque, both eyes

SD-OCT

Spectral-domain optical coherence tomography

Authors’ contributions

MLV, JMH and SAP conceived the study. AL, MLV, JMH, AKS and SAP enrolled patients in the study. AL and SAP performed the SD-OCT examinations and the vast majority of ophthalmic examinations. AKS performed the data search, tabulated, entered and cleaned the data set. SAP evaluated the SD-OCT images for quality for inclusion in the study. AKS drafted the initial manuscript and proofread and revised all materials as required. AKS and SAP created the tables and figures. AL, MLV, JMH and SAP proofread and revised the manuscript as required. All authors have made a significant contribution to the text and have approved the final version.

Funding

Department for Small Animals, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland.

Data availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Declarations

Ethics approval and consent to participate

Ethical approval was not required for this study as an ophthalmic examination is non-invasive, and a critical component of assessment for wild birds of prey presenting following suspected trauma. Similarly, SD-OCT is a non-invasive examination which has been shown to contribute significant information with regards to retinal pathology for numerous species, including birds. The SD-OCT examinations were well tolerated awake with minimal manual restraint, as necessary for routine physical and ophthalmic examinations, by all patients. Consent to participate is not applicable as these were all wild birds, with no agent/owner.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.