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Two cases of neoplasia of basal cell origin affecting the axillary region in anseriform species.

Abstract: Neoplasms of the skin are occasionally seen in domestic birds but are uncommon in nondomestic birds. An 8-year-old male hooded merganser (Lophodytes cucullatus) was presented with bilateral axillary ulcerative lesions that improved but did not resolve with empiric antibiotic and antifungal therapy. Skin biopsies were taken, and bilateral feather folliculomas were diagnosed on histopathologic examination. The duck was euthanatized because of the poor prognosis. A 9-year-old Indian runner duck (Anas platyrhynchos) was presented with an ulcerative lesion, with pseudomembrane and serocellular crust affecting the axillary region. This mass was diagnosed as a basosquamous carcinoma. The mass was surgically excised, and no recurrence was observed. Feather folliculomas are usually considered benign neoplasms in domestic birds and may be primarily ulcerative, exudative, bilateral, and symmetric in location. Basosquamous carcinoma may have a similar gross appearance. It is unknown if the axillary region may be an area with increased incidence of neoplasia in birds. This appears to be the first report of feather folliculoma and basosquamous carcinoma in Anseriforme species. Feather folliculomas and other neoplasms, such as basosquamous carcinoma, should be considered as a differential diagnosis in ulcerative or proliferative skin lesions in birds.

Key words: axilla, feather folliculoma, neoplasia, basosquamous carcinoma, waterfowl, avian, hooded merganser, Indian runner duck, Lophodytes cucullatus, Anas platyrhynchos

Clinical Report

Case 1

An 8-year-old male hooded merganser (Lophodytes cucullatus) was presented to the veterinary hospital at the Maryland Zoo in Baltimore for abnormal ambulation while in its enclosure. Results of physical examination revealed bilateral moist, ulcerative dermatitis of the axillary regions, with the lesions on the right side more severe than those on the left. The plumage over the wings was of poor quality, and the right wing previously had been pinioned distal to the carpus. Otherwise, the duck was in good body condition (2.5/5 body condition score), with a weight of 552 g, which was within the reference range. (1,2) The bird was admitted to the hospital for treatment. Enrofloxacin (10 mg/kg IM; Baytril 2.27%, Bayer Healthcare LLC, Shawnee Mission, KS, USA) was administered, the lesions were cleaned with chlorhexidine scrub, and 1% silver sulfadiazine cream was applied topically. Differential diagnoses were bacterial or fungal dermatitis, trauma from an unknown source, chemical or other irritation, and neoplasia. Treatment with enrofloxacin (20 mg/kg PO q24h) and Bene-bac (1 g PO q24h; PetAg, Hampshire, IL, USA) was instituted, along with daily topical cleaning of the lesions with dilute chlorhexidine and application of silver sulfadiazine cream. Cytologic examination of a swab sample of the lesion taken before topical treatment revealed numerous epithelial cells with few pleomorphic bacteria, rare white blood cells, and no fungal elements.

The lesions initially improved with treatment, and the bird was returned to the aviary after 10 days, with near resolution of the lesion that affected the left wing and substantial improvement of the lesion that affected the right. The bird was re-examined 3 days after its return to the aviary, at which time the lesions appeared worse. The bird was returned to the veterinary hospital for further diagnostic testing and treatment. Antibiotic therapy was changed from enrofloxacin to trimethoprim-sulfamethoxazole (30 mg/kg PO q 12h) and 1% itraconazole (10 mg/kg PO q24h; Sporonox; Ortho-McNeil, Raritan, N J, USA) was added to the treatment regimen. During the course of treatment, the plumage became increasingly tattered, with poor feather quality (Fig 1).

[FIGURE 1 OMITTED]

Because of the lack of resolution, skin biopsy samples were taken with a 4-mm biopsy punch from both the left and right axillary areas. The skin could not be closed after the biopsy because of the ulcerative nature of the lesion and extremely friable skin edges (Fig 1). Granulation tissue was present at the lesion. Results of histologic examination of the biopsy sample from the right axillary region showed nodules of neoplastic and inflammatory cells (Figs 3 and 4). The neoplastic cells were arranged in cords and nests, separated by variable amounts of fibrous or loose connective tissue. The cells were polygonal, with distinct boundaries; moderate amounts of eosinophilic cytoplasm; and round-to-oval nuclei, with finely granular cytoplasm. Moderate anisocytosis and anisokaryosis were present and mitotic figures were uncommon. The neoplastic cells were mixed with abundant heterophils and discrete nodules of lymphocytes. The overlying epidermis showed hyperkeratosis, with intracorneal heterophils, hemorrhage, and mucinous material.

Although histopathologic results identified a neoplasm of basal cell origin, a second skin biopsy was done to confirm the diagnosis. Results of the second biopsy confirmed the presence of a basal cell neoplasm consistent with feather folliculoma in both the left and right axillary lesions. The bird was euthanatized.

At necropsy, a focal area of ulceration and crusting (10 x 5 mm) was present on the medial surface of the right proximal humerus and extended into the axilla. The lesion on the left was similar but smaller (5 mm x 5 mm). The only other notable necropsy finding was 2 pieces of twine (5 and 6 cm) in the ventriculus, considered an incidental finding. Results of histologic examination of the axillary lesions were similar to biopsy results: nests of neoplastic basal cells in the dermis, mixed with lymphoplasmacytic inflammation. The overlying epidermis was ulcerated and covered by a serocellular crust that contained abundant bacterial colonies. No evidence of neoplasia was found in any other organs, and the only other histologic findings were mild lymphoplasmacytic conjunctivitis and hepatitis.

Case 2

An approximately 9-year-old male Indian runner duck (Arias platyrhynchos), weighing 1.55 kg, was presented for moist dermatitis of the left axillary region. On physical examination, a 4.5cm-diameter lesion of thickened skin covered by a white pseudomembranous plaque extended from the proximal humerus, across the axilla, and along the thoracic body wall. Other than the described lesion, the duck appeared in good health and body condition. A blood sample was drawn from the right jugular vein for a complete blood count and plasma biochemical analysis, which revealed a leukocytosis (32 450 cells/[micro]l; reference range, 7720-21 567 cells/[micro]l) and hyperglobulinemia (3.4 g/dl; reference range, 1.7-2.9 g/ dl). (1) Samples were taken for cytologic examination as well as for bacterial and fungal culture. Enrofloxacin (15 mg/kg IM initially, then 15 mg/ kg PO q24h; Baytril) was administered. Results of cytologic examination revealed primarily grampositive cocci and squamous epithelial cells. Bacterial culture produced a heavy growth of A cinetobacter calcoaceticus-baumanii, Escherichia coli, and Proteus" mirabilis, and moderate growth of a Bacillus species, whereas results of fungal culture were negative. All bacterial organisms were susceptible to enrofloxacin, so oral treatment was continued, although heavy growth of multiple organisms made contamination likely.

[FIGURE 2 OMITTED]

The next day, the duck was anesthetized to debride and biopsy the lesion. Anesthesia was induced with 5% isoflurane administered by face mask, followed by intubation and anesthetic maintenance on 3% isoflurane. Feathers were plucked from the affected area, and the lesion was debrided with dry gauze, followed by a chlorhexidine scrub. Two wedge biopsy samples were taken from the thickened lip of the dorsal edge of the lesion. A nonadherent pad (Telfa, Kendall Co, Mansfield, MA, USA) was placed over the lesion, and the area was bandaged. Enrofloxacin was continued, and meloxicam (0.2 mg/kg IM initially, followed by 0.1 mg/kg PO q24h; Metacam, Boehringer Ingelheim Vetmedica, St Joseph, MO, USA) was administered for 3 days after surgery.

Biopsy results revealed basosquamous carcinoma, with ulceration and heterophilic inflammation. Neoplastic cells were cuboidal to polygonal, with variable degrees of squamous differentiation and cornification toward the center of nests. Moderate anisocytosis and anisokaryosis and mitotic figures were variable (0-4 per high power field). The surface epidermis was multifocally ulcerated, with areas of hemorrhage and infiltrates of heterophils. Neoplastic cells extended to the margins of the wedge biopsy.

Ten days after initial presentation, the duck was anesthetized again, and complete resection of the mass was attempted. The mass was tightly adhered to underlying musculature, especially along the body wall. Only 5-8-mm lateral margins were obtained during resection, and one muscle plane depth was achieved along the dorsal body wall by transecting the latissimus dorsi muscle. Skin closure was achieved with 4-0 polydiaxanone (PDS II, Ethicon, Inc, Somerville, N J, USA) in a simple interrupted near-far-far-near tension-relieving pattern. The surgical site was bandaged with a wing to body wrap. Meloxicam and enrofioxacin were given at previous dosages for 3 days and 10 days, respectively. Healing was complete.

[FIGURE 3 OMITTED]

Biopsy results revealed an unencapsulated, invasive, expansile, moderately cellular mass composed of nests and packets of well-differentiated squamous cells on a fine fibrovascular stroma, often widely separated by an abundant collagenous stroma. Centrally, many of the nests of cells contained amorphic globules of a bright eosinophilic material consistent with keratin. Cells were cuboidal to polygonal in shape, with moderate amounts of foamy eosinophilic cytoplasm, well-defined cellular borders and roundto-oval nuclei, with coarsely clumped chromatin and a prominent central nucleolus (Figs 5 and 6). Approximately 1-4 mitotic figures per high power field were seen. Neoplastic cells extended well into both the deep and lateral margins. The epidermis was multifocally ulcerated and covered by a serocellular crust, with variable amounts of predominantly heterophilic inflammation. Based on the invasion of the surrounding tissue and extension of neoplastic cells to the surgical margins, the prognosis regarding recurrence and the possibility of metastasis was guarded to poor. By 3 months after surgery, however, the duck had regained full use of its wing, with no recurrence of the mass.

Discussion

Neoplasia of the skin is fairly common in pet birds and chickens but rare in free-flying wild and captive wild (zoo or aviary) birds. The 2 anseriform species in this report had a unique presentation of axillary neoplasia of basal cell origin. The specific cause of axillary region neoplasia is unknown, although previous skin trauma has been suggested as a predisposing factor. Although in both cases we described, the birds had no known trauma to the axillary skin, the axillary region is a high-motion area and the possibility of trauma exists. In the first case, initial improvement on antibiotic treatment was likely a result of concurrent bacterial infection secondary to the ulcerative nature of the neoplasm. The initial improvement on antibiotics delayed biopsy and thus diagnosis of the neoplasm. Neoplasia was considered as a differential diagnosis in both cases, although less likely than an infectious cause or trauma, because of the bilateral, almost symmetrical distribution in case 1, as well as the ulcerative nature of the lesions in both ducks. Definitive diagnosis of dermatologic conditions frequently requires histopathologic examination despite initial improvement on antibiotic therapy, because many conditions are complicated by secondary bacterial infections. (3) The gross appearance of neoplastic diseases that affects the skin of birds can be quite varied and frequently requires biopsy to distinguish from nonneoplastic conditions.

[FIGURE 4 OMITTED]

The general poor feather quality of the merganser in case 1 may have been another indication of disease. The lack of preening and stress may be contributing factors, although the cage mate brought to the veterinary hospital for companionship demonstrated no loss of feather quality. It was later thought that the neoplasm or chronic discomfort may have affected the bird's plumage in general. A bird's skin and feather quality can indicate of its general health and environmental condition. (4)

[FIGURE 5 OMITTED]

Reports of neoplasia rates in captive wild birds are low and ranged from 1.0% to 3.1% in a study that collected necropsy data from 3 major U.S. zoos? Necropsy data from one zoo indicated that epithelial tumors were the most commonly reported type for both malignant and benign tumors in avian species. However, from 1901 to 1955, only 2 benign epithelial tumors were found in Anseriformes; the specific type was not listed. (6) Integumentary neoplasms were also the most common type in a survey of neoplasms found in species of pet birds. (7)

Feather folliculomas are considered benign integumentary neoplasms and form sheets, cords, or nests. They are similar to basal cell tumors but are associated with feather follicles. (8) Feather folliculomas were reported in pet avian species and are described as well-circumscribed, elevated, broad-based, epidermal lesions that generally respond well to surgical excision but may recur locally. (9,10) They are distinguished from other skin neoplasms by exhibiting evidence of feather differentiation. A feather folliculoma was diagnosed in a captive-bred barn owl (Tyto alba), with a proliferative mass that affected the left wing. (11) In this case, the lesion was described as protuberant, hard, gray, and unencapsulated, very different than the gross appearance of the lesions that affected the merganser we described.

Basal cell tumors, which have a similar gross and histopathologic appearance to feather folliculomas, were reported in a blue-fronted Amazon parrot (Amazona aestiva) and were bilateral. (12) Tumors of basal cell origin in birds are not very well defined or classified (R. Montali, written communication). Basosquamous cell carcinoma is a variant of basal cell carcinoma that has features of both basal cell and squamous cell carcinoma. This variant tends to be more locally invasive and less well circumscribed than basal cell tumors but is not as aggressive as squamous cell carcinoma. (13) To our knowledge, this is the first case report of a basosquanaous cell carcinoma in an avian species.

[FIGURE 6 OMITTED]

Treatment generally suggested for neoplasms of basal cell origin is surgical excision. Surgical excision is the most common treatment of neoplasia in birds in general. (14) In the first case, however, complete surgical excision was not considered possible because of the ulcerative nature of the neoplasm as well as the lack of remaining viable skin to close the defects. The remaining skin in the area was extremely friable and could not be closed after a 4-mm punch biopsy was taken. The right wing would have likely required amputation to remove most of the lesion, but this was not considered a viable option, because surgical treatment alone would not be curative. Although feather folliculomas are generally considered benign, the large, ulcerative lesions could not be adequately treated in this case, and the bird was euthanatized. In the second case, surgical excision was attempted, and, although clean margins were not achieved, no recurrence has been noted thus far. Amputation of the wing was considered but declined by the animal care staff because the duck was used for education purposes and was of advanced age. Because the neoplasm extended from the base of the wing on to the skin of the body, amputation would likely not have been curative in this case either.

Other therapies used to treat neoplasia in birds are radiation, chemotherapy, and photodynamic therapy. Radiation has been used to treat squamous cell carcinomas in avian species with some success; however, radioresistance is common. (15) Although feather folliculomas may be responsive to radiation, they are generally able to be surgically resected, and, thus, no published information could be found regarding radiation therapy of feather folliculomas. In case 1, extensive therapy would have been stressful to the bird, because it came from a free-flight aviary and was unaccustomed to handling. Because of the poor long-term prognosis and easily stressed nature of the patient, treatment was not attempted and euthanasia was performed after definitive diagnosis.

To our knowledge, these are the first reports of a folliculoma and basosquamous carcinoma in an anseriform species. Neoplasia of basal cell origin should be considered as a differential diagnosis in birds with diffuse, ulcerated axillary skin lesions, even those that initially respond to antibiotic treatment.

Acknowledgments: We thank Richard Montali, DVM, Dipl ACVP, Dipl ACZM, and David L. Huso, DVM, PhD, for assistance with the histopathology. We also thank the animal care and hospital staff at the Maryland Zoo in Baltimore for their assistance with the clinical aspects of the case.

References

(1.) Teare JA, ed. Reference Ranges for Physiological Values of Captive Wildlife [book on CD-ROM]. Eagen, MN: International Species Identification System; 2002.

(2.) Dunning JB, ed. CRC Handbook of Avian Body Masses. 2nd ed. Boca Raton, FL: CRC Press; 2008:25.

(3.) Latimer KS. Oncology In: Ritchie BW, Harrison G J, Harrison LR, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers; 1994:644.

(4.) Lamberski N. A diagnostic approach to feather picking. Semin Avian Exotic Pet Med. 1995;4:161-168.

(5.) Dillberger JE, Citino SB, Altman NH. Four cases of neoplasia in captive wild birds. Avian Dis. 1987;31:206-213.

(6.) Lombard LS, Witte EJ. Frequency and types of tumors in mammals and birds of the Philadelphia Zoological Garden. Cancer Res. 1959;19:127-141.

(7.) Leach MW. A survey of neoplasia in pet birds. Semin A vian Exotic Pet Med. 1992; 1:52-64.

(8.) Schmidt RE, Reavill DR, Phalen DN. Pathology of Pet and Aviavy Birds. Ames, IA: Iowa State Press; 2003:191.

(9.) Koski MA. Dermatologic diseases in psittacine birds: an investigational approach. Semin Avian Exotic Pet Med. 2002;11:105-124.

(10.) Schmidt RE, Lightfoot TL. Integument. In: Harrison G J, Lightfoot TL, eds. Clinical Avian Medicine. Vol. 1. Palm Beach, FL: Spix Publishing; 2006:405-406.

(11.) Frasca S, Schwartz DR, Moiseff A, French RA. Feather folliculoma in a captive-bred barn owl (Tyro alba). Avian Dis. 1999;43:616-621.

(12.) Tell EA, Woods L, Mathews KG. Basal cell carcinoma in a blue-fronted Amazon parrot (Amazona aestiva). Avian Dis. 1997;41:755-759.

(13.) Jones TC, Hunt RD, King NW. The skin and its appendages. In: Veterinary Pathology. 6th ed. Baltimore, MD: Williams & Wilkins; 1997:855.

(14.) Quesenberry K. Treatment of neoplasia. In: Altman RB, Clubb SL, Dorrestein GM, Quesenberry K, eds. Avian Medicine and Surgery. Philadelphia, PA: WB Saunders: 1997:600-602.

(15.) Lightfoot TL. Overview of tumors: Section 1. In: Harrison G J, Lightfoot TL, eds. Clinical Avian Medicine. Vol. 1. Palm Beach, FL: Spix Publishing; 2006:561.

Carol Bradford, DVM, MS, Allison Wack, DVM, Sarah Trembley, DVM, Teresa Southard, DVM, PhD, and Ellen Bronson, Med Vet, Dipl ACZM

From the Maryland Zoo in Baltimore, Druid Hill Park, Baltimore, MD 21217, USA (Bradford, Wack, Bronson), and the Department of Molecular and Comparative Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA (Trembley, Southard).
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Title Annotation:Clinical Reports
Author:Bradford, Carol; Wack, Allison; Trembley, Sarah; Southard, Teresa; Bronson, Ellen
Publication:Journal of Avian Medicine and Surgery
Date:Sep 1, 2009
Words:3018
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