Veterinary Ophthalmology (2017) 20, 6, 496–504 DOI:10.1111/vop.

12453

The consequences of avian ocular trauma: histopathological

evidence and implications of acute and chronic disease
Bret A. Moore,*,1 Leandro B. C. Teixeira,† William E. Sponsel‡§ and Richard R. Dubielzig†
*Department of Biological Sciences, Purdue University, 915 W. State Street, West Lafayette, IN 47907, USA; †Department of Veterinary Pathological
Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 3374 Veterinary Medicine Building, 2015 Linden Drive, Madison, WI 53706,
USA; ‡Departments of Biomedical Engineering, University of Texas San Antonio, One UTSA Circle, San Antonio, TX 78249, USA; and §Vision Sciences,
University of the Incarnate Word, 311 Camden Street, San Antonio, TX 78215, USA

Address communications to: Abstract

B. A. Moore
Tel.: (530) 752-3937
Fax: (530) 752-6042
e-mail balmoore@ucdavis.edu
1
Present address: ATTN:
Ophthalmology, Room 229
School of Veterinary Medicine
University of California-Davis 1
Garrod Drive Davis, CA 95616
USA
[Corrections added on 20 Jan-
uary 2017, after first online
publication: the telephone
number, email, and present
address of the corresponding
author have been changed
from +1 317 294 5691,
bretthevet@dvm.com, and
Veterinary Specialty Hospital
of San Diego, 10435 Sorrento
Valley Road, San Antonio,
CA, 92121, USA to (530) 752-
3937, balmoore@ucdavis.edu,
and ATTN: Ophthalmology,
Room 229 School of Veterin-
ary Medicine, University of
California-Davis, 1 Garrod
Drive, Davis, CA 95616,
USA, respectively.]
Objective To present a description and categorization of the histopathological lesions
in avian ocular trauma.
Animal studied Seventy-five birds diagnosed with ocular trauma at to the Comparative
Ocular Pathology Laboratory of Wisconsin.
Procedures Histological slides were reviewed, and the type of trauma was classified by
cause into either (i) blunt trauma or (ii) penetrating trauma and by duration into
(i) acute or (ii) chronic.
Results Blunt trauma was the most common source of trauma, and the most frequent
lesions were observed in the retina (91%), with 71% of retinas having a tear or
detachment and 46% of retinas showing chronic degenerative changes. Damage to the
iris/ciliary body was present in 77% of cases. Corneal (17%) and lens (31%) lesions
were relatively low. Acute traumatic events had a higher prevalence of readily identifi-
able discrete retinal tears/detachments (64%). Nearly all cases of chronic trauma
exhibited chronic retinal lesions (93.7%), as well as a greater percentage of cartilage/
bone lesions (71.4%), irido/cyclodialysis (51.9%), lenticular lesions (72.7%), and cor-
neal damage (83.3%). However, the incidence of iridocyclodialysis was roughly equiva-
lent for acute and chronic blunt trauma.
Conclusions Ocular trauma can lead to profound acute and chronic lesions within the
eye. Here, we provide insight into understanding ocular damage caused by trauma,
which may help future studies suggest new therapeutic options and provide insight
regarding the releasability of avian wildlife.
Key Words: avian, bird, blunt trauma, chronic, eye, injury

habitats and visual backgrounds,3,8–10 variable activity

INTRODUCTION
Most avian species depend on vision, whether as a means
of social interaction in pet birds or for gathering informa-
tion critical for survival of those living in the wild.1–3 The
unique combination of perceptual challenges that the
visual system of different birds face may have been a driv-
ing force in the development of distinctions in the visual
systems of birds from those of other vertebrate clades.
Such challenges include flight,4–6 the need to find and
acquire specific types of food,7 variable structure of
patterns,11 and for reproductive behaviors and sexual
selection.12–16 As a result, the eyes of birds possess several
features that are conserved across the avian taxa, including
large globe volume for respective body mass,17,18 dispro-
portionally large posterior segment,18–20 the presence of a
vascular intraocular pecten, an annular pad and strong cil-
iary attachment to lens,21 accommodation by corneal and
lenticular measures, an avascular retina, scleral ossicles
and cartilage,18,22,23 a relatively thin cornea,20–24 and com-
plete decussation of optic nerve fibers. Although beneficial

© 2017 American College of Veterinary Ophthalmologists


to the lifestyle of birds, this combination of ocular features
may also contribute to pathologic processes in response to
ocular trauma, which may in turn impact vision and ulti-
mately survival.25
Ocular disorders are relatively common findings among
birds, particularly those that are free-living. Holt and
Layne25 showed that 2.05% of wild-trapped owls had pre-
vious ocular abnormalities visible by standard ophthalmic
examination, and Murphy et al.26 suggested that 15% of
ill or injured birds received at rehabilitation centers or
veterinary clinics had ocular lesions. In wild birds, ocular
trauma is noted as a frequent cause of ocular morbidity
(more than 30%).25,27–29 Even among captive raptors that
were originally deemed unreleasable due to injuries unre-
lated to the eyes, ocular lesions have been found in 50%
of the eyes examined.30 Overall, trauma is said to be
responsible for nearly 90% of eye disorders diagnosed in
wild raptors,26,27 and ocular trauma is considered the most
common cause of ocular morbidity in wild birds of
prey.26,27,31–33
The clinical features of traumatic damage to the avian
eye have been characterized.26,27,34–37 However, most
studies evaluating ocular disease birds with suspected
trauma have primarily focused on the clinical evaluation of
wild and pet birds.25,26,32,34,36,37 Fewer reports of the use
of advanced diagnostics have been published (e.g., elec-
troretinogram and B-mode ultrasound,36 optical coherence
tomography).38 One report mentioned on the histopatho-
logic findings of euthanized birds in a primarily clinical
study; however, the majority of eyes were normal and the
discussion of histopathology was limited.36 Overall,
despite a growing body of clinical reports on avian ocular
trauma, there has been little work regarding the compara-
tive histopathologic description and classification of ocular
trauma in birds.25 Our aim here was to present a descrip-
tion and categorization of the histopathological lesions in
avian ocular trauma, which has important implications to
understanding traumatic pathology to the eye and may
provide insight into understanding hazards leading to ocu-
lar trauma. As a result, future studies may be able to sug-
gest new diagnostic and therapeutic options for ocular
trauma and, in wild birds, provide insight regarding the
releasability of avian wildlife.
MATERIALS AND METHODS
The histology and submitting records from all birds diag-
nosed with ocular trauma at the Comparative Ocular
Pathology Laboratory of Wisconsin (COPLOW) between
1990 and 2014 were reviewed. Avian samples were
received from a wide range or institutions, including but
not limited to universities, zoos, private ophthalmology
and general veterinary practices, and wildlife rehabilitation
centers. Most samples were from wild-caught or captive
birds that were once free-living, but a few samples were
most likely from pets based on the species and from where
© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504
avian ocular trauma 497
they were submitted. Evidence of ocular trauma was
determined by the referral information or the histopatho-
logical features suggestive of a traumatic event. All slides
were reviewed to confirm the presence of lesions sugges-
tive of trauma. All referral clinical information was
obtained from the submission forms by the referring vet-
erinarian or party, or by personal communication. There
are a total of 881 avian globes in the COPLOW collec-
tion. Most of these are normal, and 75 have lesions sug-
gestive of trauma.
Globes submitted to COPLOW were fixed in either
Davidson’s solution or 10% neutral buffered formalin and
were decalcified prior to being sectioned in a parasagittal
plane (mostly dorsoventral) upon arrival, followed by pro-
cessing for 5-lm sectioning of paraffin blocks and routine
staining with hematoxylin and eosin (H&E). Special stains
were occasionally requested following examination of a
H&E-stained slide, such as alcian blue periodic acid–
Schiff (PAS), to further characterize structures or particu-
lar interest.
We classified the type of trauma into one of the two
categories listed below. The classifications were based on
referral clinician submission forms or histopathologic fea-
tures. The two categories were (i) blunt trauma or
(ii) penetrating trauma. Cases of blunt trauma were further
classified by duration of disease (e.g., acute and chronic).
When assessing the duration of a disease process by
observing the tissue reaction histologically, the best that
can be achieved is to estimate the least amount of time
required to manifest the tissue changes observed. In this
case series, we consider 10 days or longer to be chronic
disease, and therefore, we evaluated the tissue for changes
that require at least 10 days to develop. Below we list the
changes used to determine acute from chronic disease in
the tissues or the globe. Acute lenticular disease was con-
sidered in cases with lens capsule rupture and fiber disrup-
tion with no cellular response, or simple lens epithelial
cell clustering and small numbers of phagocytic cells.
Chronic lenticular disease was described as lens epithelial
cell fibrous metaplasia, mineralization, or extensive phago-
cytosis of lens fibers. Trauma to the anterior uvea was
considered acute where there was separation of tissue with
hemorrhage, but no remodeling, and chronic when
remodeling and fibrosis of the torn surfaces, or synechia,
were noted. Acute retinal trauma was described as jumbled
tissue but no cellular reaction or detachment, and damage
to the photoreceptor cells with hemorrhage or small num-
bers of phagocytic cells. Chronic retinal trauma was
described as remodeling of the torn retina, profound atro-
phy, or lenticular metaplasia.
RESULTS
Our dataset on avian ocular trauma consisted of 27 spe-
cies. Most of the avian cases considered to be consistent
with traumatic ocular damage were raptors, with over half
498 moore ET AL.
Figure 1. Distribution of species in cases used in the study (n = 75).
of those being owls. Hawks and eagles made up nearly
one quarter of the cases, whereas fewer falcons (1), parrots
(5), waterfowl (2), and other groups of species (11, includ-
ing songbirds, chickens and pheasants, hornbills, a bus-
tard, a heron, a roadrunner, and a penguin) were
represented (Fig. 1).
Penetrating trauma
The lesions seen in the four penetrating trauma cases were
variable. In two cases, remnants of the foreign material
were found in the eye: a thorn embedded in the lens
(Fig. 2), and a feather embedded in the episcleral tissue.
Other findings in eyes with penetrating trauma included
corneal disease, lens rupture or cataract, retinal traumatic
degeneration, retinal detachment, and retinal lenticular
metaplasia (Fig. 3a).
Blunt trauma
Blunt trauma was seen in the majority of cases examined.
A wide range of lesions were seen and were most fre-
quently observed in the retina as retinal tears or detach-
ments, or less commonly as evidence of chronic
degeneration. Damage to the iris/ciliary body was also a
frequent finding, all being represented as irido/cyclodialy-
sis. Corneal and lens damage was relatively low compara-
tively (Fig 3b).
Acute vs. chronic blunt trauma pathology
Acute and chronic cases of blunt trauma were approxi-
mately evenly represented (Fig. 4). Nearly all samples of
(a) (b)
© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504
acute trauma showed evidence of retinal tears or detach-
ments (Fig. 5a). Fragmentation of the photoreceptor inner
and outer segments along with hemorrhaged and a phago-
cytic response was a common feature in the acutely dam-
age retina associated with a blunt traumatic event
(Fig. 5b). Acute iridocyclodialysis was also frequently doc-
umented (Fig. 5c). Trauma to cartilage/bone, lens, and
cornea were less common (Fig. 4a). Chronic retinal
changes were noted in one case, likely a result of prior
traumatic ocular damage. Among eyes with predominantly
chronic blunt injury, retinal damage and iridocyclodialysis
were the most common lesions noted (Fig 6a). Iridocycli-
tis was represented similarly in both acute and chronic
cases. However, chronic retinal degenerative changes were
seen far more frequently (Fig. 6b). Retinal lentoid meta-
plasia was seen in approximately one-third of cases with
chronic changes. Identifiable discrete retinal tears and
detachments were common but less frequent than in acute
cases. Furthermore, a greater incidence of cartilage/bone,
lens, and corneal lesions was noted (Fig. 4b).
DISCUSSION
Species distribution
These results support previous observations that owls may
be more prone to ocular injury than other raptors.25,33
Murphy et al.26 showed that five of the seven most com-
mon species incurring ocular injuries out of 931 birds
examined were species of owls. Our results show that
more than 50% of ocular trauma cases were in owls (see
Fig. 1). Murphy et al.26 and Murphy39 also suggested that
owls may be more prone to develop cataracts as a result of
ocular trauma but the present study does not address the
case of cataract alone. Owls have several distinct anatomic
features that may explain their bias toward eye trauma.
First, owls have relatively flat faces, and more frontally
positioned eyes16 when compared to other birds. Because
of this, blunt trauma to the eye may occur more fre-
quently with collision-type accidents, because the eyes are
more exposed and less protected by the topography of the
head. Second, the eyes of owls protrude forward from the
head due to their tubular shape and large curved cornea
and may be an initial striking point in blunt trauma cases.
Finally, the large globe:orbit ratio limits the presence of
extraocular muscles and other orbital soft tissues. The eyes
Figure 2. (a) Photomicrograph of the lens of a
red-tailed hawk with penetrating trauma. There is
a cactus thorn foreign body embedded in the lens
tissue, (b) thorn viewed under polarized light.

Figure 3. (a) Distribution of intraocular lesions
in cases of known penetrating trauma (n = 4) and
b) distribution of intraocular lesions occurring in
cases of known blunt traumatic events, further
categorized as acute and chronic (n = 36).
fit tightly within the boney orbit limiting the relative vol-
ume of shock absorbing soft tissues within the orbit.
However, other causes for having reported a higher per-
centage of raptors sustaining ocular trauma compared to
other avian species cannot be excluded based on our
results. For example, raptors may have an increased
chance of survival until being found due to having fewer
predators than other birds as raptors are predators them-
selves. They may also have an increased chance of being
found due to their large size. Finally, potentially increased
interest in preservation or rehabilitation of raptors com-
pared to other wild avian species may result in more rap-
tors being presented to veterinary clinics or rehabilitation
centers.
Studies suggest that blunt trauma, as would occur dur-
ing collisions, is the most common traumatic injury in
© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504
avian ocular trauma 499
birds.26,28,33,34,36,40 Labelle et al.36 suggested that ocular
lesions in hawks and owls were primarily associated with
head trauma (86.7%), and fewer lesions were noted in the
eyes of birds sustaining body trauma (41.9%), having sys-
temic disease (50%), or in healthy birds (20%).36 In a clin-
ical case series, Seruca et al.27 examined the effects of
blunt trauma in the eyes of two owl species. Lesions
occurred in 27% of traumatized owls, and the distribution
of lesions was similar to those reported in the present
study: cataracts (11.1–18.6%), retinal detachment (5.6–
10.5%), iridocyclitis (23.3–27.8%), corneal erosion/ulcer
(12.8–57.4%), and chorioretinitis (42.6–53.5%).27 Cases
confirmed as chronic ocular lesions (bird sustained ocular
damage > 6 weeks prior) were examined clinically by Wil-
liams et al.,35 who also reported similar findings among
birds with all forms of trauma, although among their
500 moore ET AL.

Figure 4. Distribution of intraocular lesions in

cases of (a) acute (n = 17) and (b) chronic blunt
trauma (n = 19).

(a) (b) (c)

Figure 5. Select acute lesions following blunt ocular trauma. (a) Gross photograph of a retinal tear (arrows) near the pecten due to acute
trauma in an eagle, (b) acute trauma pattern outer retinal degeneration and phagocytosis (asterisks) in an owl, (c) acute trauma showing
cyclodialysis (arrow) and an area of acute trauma pattern retinal degeneration (asterisk) in an owl.

cohort, more fibrosis and other chronic changes were seen trauma cases is too small to draw accurate comparative
(e.g., preretinal fibrotic membranes in 34% of eyes). Our conclusions, but greater propensity for the development of
results suggest that blunt trauma results in damage to sim- fibrotic membranes would be expected in open globe
ilar ocular structures. Our sample size of penetrating injuries.

© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504


(a)
Figure 6. Select chronic lesions following blunt
ocular trauma. (a) Chronic trauma with retinal
tears, detachment, atrophy, and cataract in an
owl, (b) chronic traumatic retinal degeneration (*)
in a pelican.
It is clear from previous clinical studies that different
ocular components can be damaged as a result of trau-
matic injury, and at different frequencies. Davidson34
described the ocular components damaged during trau-
matic events that could be detected in the live animal via
ophthalmic examination. Scleral ossicles and scleral carti-
lage are not easily evaluated by direct examination in trau-
matic injury to the eye.26,39,41 Anterior uveitis (including
hyphema)32,36 and secondary cataracts26,39 are among the
most common ocular findings. The avian cornea is rela-
tively spared in traumatic injury in many reports;34,39
however, some have reported a relatively high number of
corneal abnormalities.36,37 Lens displacement is not often
reported, perhaps due to the tight attachment of the cil-
iary processes to the lens annular pad.34 Hyphema may be
related to bleeding from a ruptured iris or ciliary body.
Interestingly, iridocyclodialysis is also not a common find-
ing on clinical evaluation.34 Finally, the posterior segment
is often difficult to assess due to opaque media in a trau-
matized eye. Intravitreal hemorrhage is common, possibly
because of bleeding from the vascular pecten.26,32,36,37,42
Retinal tear or detachment is a common finding when
visualization of the retinal is not obscured by anterior seg-
ment or vitreous opacities.34,36
Cornea
There was a low frequency of corneal damage in the series
of cases presented here, supporting the results of previous
clinical surveys. There is evidence suggesting that the cor-
nea in birds responds to injury differently than in
mammals.22 One study presents evidence that the avian
cornea resists the formation of stromal vascularization or
pigment infiltration.39 Our data reaffirms this; fewer than
20% of birds in this survey of blunt traumatic eye disease
demonstrated histological evidence of corneal lesions
(Fig. 3b). This is interesting considering that the cornea is
the principle ocular structure in contact with the external
environment. One reason that the cornea may be relatively
resilient is a result of the malleable properties of the cor-
neal tissue relative to the rest of the avian sclera. Periph-
eral to the cornea, boney ossicles, and cartilage that nearly
© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504
avian ocular trauma 501
(b)
encompass the globe may efficiently resorb energy trans-
ferred from the cornea.34
Scleral ossicles and cartilage
The damage to the eye from a blunt traumatic event is
related to the physical and anatomic structure of the
globe. The integration of scleral ossicles and cartilage pro-
vides a more rigid structure to the avian eye than exists in
predominantly collagenous mammalian eyes. This rigidity
may also increase the risk of harm to the delicate uveal
structures, which are largely held in place by surface ten-
sion and uniform intravitreal pressure internally. If a bird
is struck on the head or impacts an obstacle in flight, the
rigid globe enhances the amount of kinetic energy trans-
mitted to the delicate uvea and retina. Blunt trauma can
result in a coup/contrecoup reaction and damage to inter-
nal structures such as the uvea or retina.34 Iridocyclodialy-
sis, retinal detachment, and retinal tear are more likely as
a consequence. Another, more subtle effect of kinetic
energy transmitted through the eye is separation of the
photoreceptor outer segments leading to outer retinal
degeneration.
Anterior uvea (iris and ciliary body)
The iris base and the ciliary body of birds are attached
to the rigid sclera at the limbus which, in turn contains
the scleral ossicle. The attachment is achieved by a deli-
cate system of thin stromal bands analogous to pectinate
ligaments. A blunt traumatic event to the outside of the
globe transmits an energy wave which displaces the lens
creating a shearing force, which disrupts the integrity of
the vulnerable attachment between the ciliary body and
the sclera. As a result, the iris base and ciliary body are
shorn from the sclera (iridocyclodialysis). We believe that
this relationship of the uvea to the rigid sclera explains
the frequency of iridocyclodialysis as a feature of blunt
trauma. The suspension of the lens annular pad to the
ciliary processes along with the jolt of energy acting
against the rigid sclera at the limbus can be a double
source of traction on the ciliary body following a blunt
traumatic impact.
502 moore ET AL.
Retina
Transfer of energy from the rigid sclera to the internal
structures of the eye also affects the integrity of the retina.
An energy wave propagates through the semiliquid retinal
tissues and has the effect of disrupting the most delicate
layer of the retina (i.e., the junction between the inner
and outer segments of the photoreceptors). A greater
amount of energy may damage more than the photorecep-
tors, for example, disrupt the inner retina or lead to reti-
nal a tear or avulsion of the retinal from around the
pecten. Birds have a well-defined vitreous body, which is
firmly attached around the pecten and at the ora ciliaris
retinae. These two anatomic sites are often the foci of
retinal tear in blunt trauma. Davidson34 has suggested that
the posterior structures of the eye may also be more prone
to traumatic damage because of the shape of the eye.
These types of lesions are exactly what were seen in the
present study in the globes of birds after blunt trauma
(Figs 5 and 6).
Another feature of the avian retina that may lead to an
increased risk for damage in trauma cases is the fact that
the retina is avascular. After impact, the globe expands
equatorially, destabilizing the uveoscleral interface. The
tensile integrity of the retinal vascular network imparts a
measure of support for the otherwise semiliquid retinal
tissue to resist additional shearing in the face of oscillating
lower amplitude pressure wave reflections that arise after
the initial short-duration high-amplitude shock waves
known to occur in blunt eye trauma.43 These post-impact
intraocular pressure oscillations are enhanced when free
energy release is constrained within a closely approximated
bony orbit.44 Retinal hypoxia in the detached avian retina
may be a part of the pathogenesis of chronic retinal
degeneration, especially if diffusion of nutrients from the
vascular pecten is disrupted by hemorrhage or impact.
The vascular pecten has been noted as a common location
for retinal tears to occur.34 This is supported in the pre-
sent study.
The interesting lesion of lentoid metaplasia was
noted in several retinae as has been previously
described.45–47 In all cases of lentoid metaplasia in the
present study, the ocular pathology was characterized
as being chronic degenerative, as suggested to be the
case by Zeiss & Dubielzig.47 In fact, lentoid metaplasia
was found in 40% of the retinae exemplifying changes
consistent with chronic degeneration, thus supporting a
chronic process.
Implications/conclusion
Although the morphology of most avian eyes is tuned for
high visual function, their ocular anatomy may predispose
them to rather profound effects following trauma. For
example, the large size of the globe leaving minimal
room for periocular cushion and the rigid cartilaginous
and boney sclera can both contribute to the development
of ocular damage following trauma. As shown in this
© 2017 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 20, 496–504
study, multiple intraocular structures are frequently dam-
aged following ocular trauma. The most commonly
affected structures are the retina and the anterior uvea.
The extent of the damage may be underappreciated on
ophthalmic examination, and a clinical interpretation of
an individual bird’s loss of visual function, or prognosis
for future vision, can be incomplete or inaccurate. For
example, acute or chronic lesions may be missed due to
the inability to evaluate the eye fully due to opacities
(e.g., hyphema, cataracts, vitreal hemorrhage, among
others). Even if the extent of ocular damage can be
appreciated on examination, assessment of the effect that
the damage has on vision is difficult due to (i) high visual
acuity with relatively poor understanding of differential
acuity across the retina, the function of specific retinal
specializations, and the cortical processing of a visual
image, and (ii) the variability in vision and dependency
on vision based on different ecological components (an-
tipredatory behaviors, foraging habits, ecological niche,
and dependency and interaction with other special
senses).48
Our understanding of the effects of traumatic ocular
injury on vision, our ability to clinically assess vision in
birds, and our understanding of species differences in
visual acuity, retinal specializations, cortical processing
of a visual image, and ecological demand for visual
function are all directly related to our ability to more
accurately diagnose, treat, and in the case of wild birds
assess which individuals are considered releasable. We
have provided a description and prevalence of intraocu-
lar effects caused by trauma. Future studies are neces-
sary and recommended to determine the impact that
these effects have on the visual capabilities of pet an
free-living birds, and how specific lesions affect
releasability of a given free-living species. Future studies
should also assess whether advanced diagnostics (e.g.,
optical coherence tomography, ultrasound pachymetry,
confocal microscopy, electroretinogram, among others)
are more likely to portray more accurate clinical pic-
tures that correlate with what has been shown histologi-
cally in this study.
ACKNOWLEDGMENT
This study did not utilize financial support or grants.
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