Pathology in Practice

Reneé E. Carleton 1Department of Biology, School of Mathematical and Natural Sciences, Berry College, Mount Berry, GA 30149.

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 DVM, PhD
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Heather Fenton 2Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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 DVM, MVSc
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John A. Bryan III 2Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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 DVM, MS
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Michael J. Yabsley 2Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.
3Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602.
1Department of Biology, School of Mathematical and Natural Sciences, Berry College, Mount Berry, GA 30149.
2Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.
3Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602.

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 PhD

History

An adult great horned owl (Bubo virginianus) was found dead on a shooting preserve in Floyd County, Ga. There were no apparent traumatic injuries, but a mass on the right side of the bird's head was noticeable. The carcass was retrieved and frozen until the time of necropsy.

Clinical and Gross Findings

Initial necropsy revealed that the bird was a second-year female great horned owl in poor nutritional condition with reduced pectoral muscle mass. A featherless, soft, and freely movable pedunculated mass was attached to the dorsal aspect of the right external auditory orifice (Figure 1). The mass measured 12.45 mm at its widest point and 20.66 mm in length from the point of attachment at the auricular base to the tip. The mass did not extend beyond the subcutaneous tissues. The surface of the mass was nonulcerated and smooth with occasional crusts. The mass did not occlude the auditory canal but covered the auditory orifice when the owl was held in a normal, upright position. There were no other substantial cutaneous lesions and no musculoskeletal abnormalities. Subcutaneous, periocular, and visceral adipose tissues were virtually nonexistent or severely atrophied, and the internal organs were grossly unremarkable. The digestive tract contained no prey items or partially digested material; however, gastrointestinal helminths were present. Representative sections of the mass and other relevant tissues were preserved in neutral-buffered 10% formalin, and recovered and fixed helminths were submitted to the Southeastern Cooperative Wildlife Disease Study, University of Georgia, Athens, Ga, for further evaluation.

Figure 1—
Figure 1—

Photographs of a soft, pedunculated mass attached to the dorsal rim of the right external auditory orifice of a great horned owl (Bubo virginianus) that was found dead and in poor nutritional condition. A—When the carcass was held upright, the mass covered the external auditory orifice. B—The mass could be lifted and did not occlude the auditory canal.

Citation: Journal of the American Veterinary Medical Association 254, 12; 10.2460/javma.254.12.1407

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page

Histopathologic Findings

The dermis of the external auditory orifice was expanded by a well-demarcated, unencapsulated, round mass composed of organized collagen and fibrocytes. Multiple, linear, acicular, clear spaces were present throughout the lesion (interpreted as cholesterol clefts [Figure 2]). Small numbers of lymphocytes, plasma cells, and macrophages and rare multinucleated giant cells (Figure 3), along with occasional small clusters of foamy macrophages with markedly vacuolated cytoplasm (Figure 4), were scattered throughout the mass. The overlying epidermis was mildly thickened and spongiotic with occasional layers of overlaying orthokeratotic keratin in multiple locations. Results of Sudan IV staining of sections of the mass were inconclusive; no organisms were detected with Ziehl-Neelsen (acid-fast) staining. No notable findings were detected in sections of the liver, kidneys, major vessels, brain, or either auricular cavity and the surrounding bone. Additional sections of skin that had been frozen lacked any cleft formation (not shown). Multiple sections of nematodes morphologically consistent with Microtetrameres spp were present in the proventriculus and ventriculus.

Figure 2—
Figure 2—

Photomicrograph of a section of the mass from the great horned owl in Figure 1. The dermis associated with the mass is expanded by fibrous connective tissue, collagen, and acicular cholesterol clefts (asterisk). Small aggregates of lymphocytes, plasma cells, and macrophages are scattered throughout the mass. H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 254, 12; 10.2460/javma.254.12.1407

Figure 3—
Figure 3—

Photomicrograph of a deeper section of the mass from the great horned owl in Figure 1. Notice the multifocal nodular aggregates of acicular cholesterol clefts surrounded by macrophages and occasional multinucleated giant cells. H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 254, 12; 10.2460/javma.254.12.1407

Figure 4—
Figure 4—

Photomicrograph of an additional section of the mass from the great horned owl in Figure 1. At higher magnification, notice a cluster of foamy macrophages (asterisk) associated with clear clefts. H&E stain; bar = 50 μm.

Citation: Journal of the American Veterinary Medical Association 254, 12; 10.2460/javma.254.12.1407

Additional Laboratory Findings

No viruses, including West Nile virus, were isolated from a sample of brain tissue that was cultured on Vero cells. Oral and cloaca swabs underwent a real-time reverse transcription PCR assay to detect avian influenza virus, and results were negative. Recovered helminths were identified as 2 female Porrocaecum sp (most likely Porrocaecum depressum), 1 female Centrorhyncus sp, and several Neodiplostomum trematodes (either Neodiplostomum americanum or Neodiplostomum reflexum). Additional gross examination of the affected right auricular cavity revealed no additional fibromatous lesions or disruption of normal anatomic components of the head.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis: cutaneous xanthoma with multifocal, mild, lymphoplasmacytic, and histiocytic dermatitis and orthokeratotic hyperkeratosis.

Case summary: cutaneous xanthoma on the external auditory orifice of a great horned owl.

Comments

Although the cause of death for the owl of the present report was undetermined, starvation was likely a contributory factor, given the owl's poor body condition, lack of traumatic injuries, and lack of any evidence of underlying infectious disease. The intestinal parasites were considered incidental findings. Toxicological analyses were not pursued.

Emaciation as a result of unidentified causes was a common finding among great horned owls examined at the National Wildlife Health Center over an 18-year period.1 The most frequently identified cause of death in Strigiformes is trauma, followed by poisoning.1–3 Avian pox, a reasonable differential diagnosis for the mass in the bird of the present report, is occasionally identified in owls and can be associated with death when lesions are extensive or interfere with consumption of prey or perching.2,4 Other infectious diseases are less common than trauma and emaciation.1–5

Aside from avian pox, cutaneous and connective tissue masses in owls have rarely been reported; those reported include squamous cell carcinoma, mast cell tumor, histiocytic sarcoma, fibroma, and fibrosarcoma.2,6–11 In the case described in the present report, fibroma was considered as a diagnosis because the histologically detected clear clefts distributed throughout the mass could have been attributable to freeze-thaw artifact. However, the uniform appearance of the clefts associated with granulomatous inflammation warranted a diagnosis of xanthoma despite an apparent paucity of foamy macrophages and multinucleated giant cells in some areas of the mass. In additional sections of skin that had been frozen, there was no cleft formation. An unfixed section of the mass was not available for oil red O staining; therefore, fibroma could not be completely ruled out. Xanthomas and xanthomatous inflammation in various avian species, including a case involving a fledgling great horned owl, have been described.12–15 The etiopathogenesis of xanthomatosis is unknown, but trauma or a dietary association has been suggested.13 These lesions are composed of lipid deposits, which are often surrounded by abundant foamy macrophages and occasional multinucleated giant cells; typically, they develop on the dorsum, distal portions of the wings, sternum, and uropygial area.14 There are rare reports15 of lipogranulomatous papillomatous lesions associated with hypercholesterolemia and hypertriglyceridemia in birds. Antemortem blood biochemical data for the owl of the present report were not available, but on the basis of the poor nutritional condition of the bird, the lipid content was speculated to not have been elevated.

The location of a cutaneous xanthoma on the rim of the external auditory orifice of a great horned owl is unusual and, to our knowledge, has not been previously described for this species. We speculated that the location of the mass and its pendulous nature may have contributed to the owl's death through interference with its ability to forage. Acoustic location, rather than vision or olfaction, is the primary means by which owls capture prey.16 This ability is facilitated by the shape of the skull, asymmetric positioning of the ears, and ear flaps and feathering that direct and concentrate sound waves to the auditory canal. In experiments conducted in total darkness, barn owls repeatedly captured prey successfully but were unable to locate or capture prey when a cotton plug was placed into one of their ears.15 Therefore, given the location of the mass, it seems plausible that prey sounds would have been improperly reflected or blocked, thereby impeding the ability of the owl to locate food.

References

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