History
An adult 2.93-kg (6.45-lb) male bald eagle (Haliaeetus leucocephalus) was brought to a tertiary care raptor medicine and rehabilitation centera immediately after it was seen fighting with another eagle. A bystander who witnessed the fight was concerned that the wounds the eagle had sustained would be harmful and thus brought the raptor to the center.
Clinical and Gross Findings
The eagle had multiple puncture wounds to its feet, thorax, right carpus, and head, including a wound on its upper right eyelid. The eagle appeared to be blind in the right eye. The lens of the right eye was discolored, compared with the lens of the left eye, and there was concern for potential cataract formation (Figure 1). Other than the apparent blindness in the right eye and the multiple wounds, results of the physical examination of the eagle were unremarkable. A complete ophthalmic examination of both eyes was performed, which included a neuroophthalmic examination, slit-lamp microscopy, and indirect ophthalmoscopy. Neuro-ophthalmic abnormalities were evaluated in the right eye, and findings included a nonresponsive mydriatic pupil, absent menace response, and absent dazzle reflex. The ophthalmic examination of the right eye revealed an upper eyelid wound, clear cornea, and mild anterior uveitis with trace to +1 flare in the anterior chamber. The lens had no signs of opacity (no cataract), but severe opacity of the vitreous humor that prevented a fundic examination of the right eye. Results of an ophthalmic examination of the left eye were considered normal. For visualization of the posterior segments, standard transcorneal ocular ultrasonography was performed on both eyes with a 10-mHz ocular ultrasound probe.b Ultrasonographically, the right eye had an apparently normal lens, hyperechoic opacities in the vitreous humor, a swollen pecten, and retinal detachment; the left eye was considered normal.
Photographs of the right (A) and left (B) eyes of an adult bald eagle (Haliaeetus leucocephalus) that was brought to a tertiary care raptor medicine and rehabilitation center immediately after it was seen fighting with another eagle. In the right eye, notice the severe opacity (cloudy yellow color) in the vitreous humor (behind the lens). There is a wound above the right eye (arrow). The left eye appears grossly normal.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photographs of the right (A) and left (B) eyes of an adult bald eagle (Haliaeetus leucocephalus) that was brought to a tertiary care raptor medicine and rehabilitation center immediately after it was seen fighting with another eagle. In the right eye, notice the severe opacity (cloudy yellow color) in the vitreous humor (behind the lens). There is a wound above the right eye (arrow). The left eye appears grossly normal.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photographs of the right (A) and left (B) eyes of an adult bald eagle (Haliaeetus leucocephalus) that was brought to a tertiary care raptor medicine and rehabilitation center immediately after it was seen fighting with another eagle. In the right eye, notice the severe opacity (cloudy yellow color) in the vitreous humor (behind the lens). There is a wound above the right eye (arrow). The left eye appears grossly normal.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→
Case Outcome
With regard to raptors, unilateral or bilateral vision loss is important because these birds rely heavily on vision for hunting and avoidance of trauma and predation.1–3 This eagle was not considered to be a good candidate for release because of irreversible blindness in the right eye; furthermore, the bird was not classified as a good candidate for life in captivity and use as an education animal. As a result, the eagle was anesthetized with isoflurane via face mask and euthanized with an IV barbiturate overdose.
A sample of vitreous humor was obtained from the right eye via paracentesis immediately after euthanasia of the eagle and submitted for cytologic evaluation and microbial culture at a diagnostic laboratory.c The right eye was fixed in neutral-buffered 10% formalin and submitted for histologic examination by a board-certified veterinary pathologist (CMR) with expertise in ocular pathological conditions.
Cytologic and Microbiological Findings
Slide preparations of the vitreous humor obtained from the right eye underwent microscopic examination, which revealed inflammatory cells with individual and aggregated short, rod-shaped bacteria (Figure 2). The sample was poorly cellular but contained sufficient material for interpretation. Heterophils were occasionally identified, but many inflammatory cells were degenerated and could not be definitively identified. Melanin granules and aggregates of bacteria, predominantly extracellular, were present on multiple slides.
Photomicrograph of a slide preparation of a sample of vitreous humor obtained by paracentesis from the enucleated right eye immediately after euthanasia of the eagle in Figure 1. Intact erythrocytes and a degenerate heterophil (red arrow) are visible. Extracellular microorganisms (black arrow) are present. Wright stain; bar = 10 μm. Inset—Aggregates of short rod-shaped bacteria are evident. Wright stain; bar = 10 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photomicrograph of a slide preparation of a sample of vitreous humor obtained by paracentesis from the enucleated right eye immediately after euthanasia of the eagle in Figure 1. Intact erythrocytes and a degenerate heterophil (red arrow) are visible. Extracellular microorganisms (black arrow) are present. Wright stain; bar = 10 μm. Inset—Aggregates of short rod-shaped bacteria are evident. Wright stain; bar = 10 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photomicrograph of a slide preparation of a sample of vitreous humor obtained by paracentesis from the enucleated right eye immediately after euthanasia of the eagle in Figure 1. Intact erythrocytes and a degenerate heterophil (red arrow) are visible. Extracellular microorganisms (black arrow) are present. Wright stain; bar = 10 μm. Inset—Aggregates of short rod-shaped bacteria are evident. Wright stain; bar = 10 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Blood agar and MacConkey agar media were used for microbial culture of the sample of vitreous humor. The cultures yielded no microbial growth after 48 hours of incubation.
Histopathologic Findings
Histologic examination of sections of the right eye revealed severe, chronic heterophilic and granulomatous choroiditis, pectenitis, and vitritis (endophthalmitis; Figure 3). Plasma cells and heterophils were the predominant cell types in the uvea, whereas the retinal pigmented epithelium was effaced by a sheet of macrophages. The choroid was edematous with scattered hemorrhage, and the retina was subtotally necrotic. The pecten was separated from the optic nerve head by granulomatous inflammation, and the inner pecten was markedly edematous and inflamed. Vitreal exudate was largely proteinaceous, with aggregates of macrophages and necrotic heterophils. Small, extracellular clusters of short bacterial rods, which were periodic acid-Schiff reaction positive and Gram stain negative, were present in the vitreous humor, adjacent to the pecten. Histologically, there was no evidence of full-thickness penetration of the globe. Secondary lesions included regional cortical lens fiber swelling (cataract) and corneal edema.
Photomicrographs of sections of the right globe of the eagle. A—In a subgross view, notice the pecten (arrow), which is expanded by edema and an inflammatory infiltrate. The retina (arrowhead) is hypereosinophilic (necrotic) and segmentally detached. The vitreous humor is highlighted by a loose proteinaceous exudate (asterisk). H&E stain; bar = 5 mm. B—Higher-magnification view of the edematous pecten (arrow), necrotic retina (arrowhead), and vitreal exudate. Faintly granular aggregates can be seen in the vitreal exudate. H&E stain; bar = 1 mm. C—In this high-magnification view, numerous aggregates of bacteria (arrows) have a weak periodic acid—Schiff reaction. The bacteria were nonreactive to Gram staining techniques in tissue sections (not shown). The edematous pecten is to the right (asterisk). Periodic acid—Schiff stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photomicrographs of sections of the right globe of the eagle. A—In a subgross view, notice the pecten (arrow), which is expanded by edema and an inflammatory infiltrate. The retina (arrowhead) is hypereosinophilic (necrotic) and segmentally detached. The vitreous humor is highlighted by a loose proteinaceous exudate (asterisk). H&E stain; bar = 5 mm. B—Higher-magnification view of the edematous pecten (arrow), necrotic retina (arrowhead), and vitreal exudate. Faintly granular aggregates can be seen in the vitreal exudate. H&E stain; bar = 1 mm. C—In this high-magnification view, numerous aggregates of bacteria (arrows) have a weak periodic acid—Schiff reaction. The bacteria were nonreactive to Gram staining techniques in tissue sections (not shown). The edematous pecten is to the right (asterisk). Periodic acid—Schiff stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Photomicrographs of sections of the right globe of the eagle. A—In a subgross view, notice the pecten (arrow), which is expanded by edema and an inflammatory infiltrate. The retina (arrowhead) is hypereosinophilic (necrotic) and segmentally detached. The vitreous humor is highlighted by a loose proteinaceous exudate (asterisk). H&E stain; bar = 5 mm. B—Higher-magnification view of the edematous pecten (arrow), necrotic retina (arrowhead), and vitreal exudate. Faintly granular aggregates can be seen in the vitreal exudate. H&E stain; bar = 1 mm. C—In this high-magnification view, numerous aggregates of bacteria (arrows) have a weak periodic acid—Schiff reaction. The bacteria were nonreactive to Gram staining techniques in tissue sections (not shown). The edematous pecten is to the right (asterisk). Periodic acid—Schiff stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 256, 8; 10.2460/javma.256.8.879
Morphologic Diagnosis and Case Summary
Morphologic diagnosis and case summary: septic endophthalmitis in the right eye of a bald eagle.
Comments
Endophthalmitis can be caused by direct penetrating trauma or via hematogenous spread.4,5 In the case described in the present report, histologic examination of the right globe did not reveal any penetrating injuries, but the eagle had an eyelid wound that was most likely caused by penetrating trauma and could have been the source of the infection in the posterior segment of that eye. Although it is possible that this eagle had endophthalmitis as a result of hematogenous spread of infection, this was considered less likely given the lack of clinical signs and abnormal behavior indicative of systemic illness or infection.
As this case has illustrated, septic vitritis and endophthalmitis should not be ruled out even if initial microbial cultures of a sample of vitreous humor yield negative results because microorganisms may be detectable on cytologic and histologic examination of appropriate specimens. Infections with fastidious bacteria, such as Mycobacterium spp and Chlamydia spp, have been described in avian species, but those organisms may not grow well on traditional media.6 In tissue sections, periodic acid-Schiff stain can be used to detect fastidious bacteria. In addition, Ziehl-Neelsen stain can be used to identify acid-fast bacteria, including Mycobacterium spp, although this stain was not used in the case described in the present report. Because recovery of infectious organisms from specimens obtained from avian species by use of conventional culturing techniques can be challenging, cytologic evaluation of tissue or fluid samples may be a more sensitive approach for detection of fastidious organisms that may be causing infections in birds.6 A clinician should be aware that the presence of microorganisms in examined cytologic preparations can sometimes be a result of contamination; for animals that do not have gross findings to support a diagnosis of microbial infection, detection of such organisms in a cytologic sample should prompt thorough sample evaluation for contamination versus true infection. Overall, microbial culture, cytologic examination, and histologic examination of appropriate specimens used as combined investigative measures are recommended in all cases of suspected infection, whenever possible. It is important to remember that Gram staining performed on paraffin-embedded tissues does not highlight gram-negative bacteria particularly well; other staining techniques (eg, use of periodic acid-Schiff, silver, or Giemsa stains), assessment of the morphology of the organisms and patterns of associated inflammation, and other testing (eg, cytologic examination and microbial culture) should be undertaken to better characterize intralesional bacteria.
Footnotes
The Raptor Center, College of Veterinary Medicine, University of Minnesota, Saint Paul, Minn.
Ellex I3 Eye Cubed A- and B-scan ultrasound machine, Ellex, Eden Prairie, Minn.
Marshfield Labs, Marshfield, Wis.
References
1. Davidson M. Ocular consequences of trauma in raptors. Semin Avian Exotic Pet Med 1997;6:121–130.
2. Pauli A, Klauss G, Diehl K, et al. Clinical techniques: considerations for release of raptors with ocular disease. J Exot Pet Med 2007;16:101–103.
3. Kuhn SE, Jones MP, Hendrix DVH, et al. Normal ocular parameters and characterization of ophthalmic lesions in a group of captive bald eagles (Haliaeetus leucocephalus). J Avian Med Surg 2013;27:90–98.
4. Reynolds DS, Flynn HW. Endophthalmitis after penetrating ocular trauma. Curr Opin Ophthalmol 1997;8:32–38.
5. Na SK, Park KJ, Kim HJ, et al. Hematogenous endophthalmitis in a patient with candidemia. Korean J Intern Med 1997;12:242–244.
6. Speer BL. Current therapy in avian medicine and surgery. Chapters 2 and 6. St Louis: Elsevier, 2016;82–98, 311.
