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Squamous cell carcinoma of the infraorbital sinus with fungal tracheitis and ingluvitis in an adult Solomon eclectus parrot (Eclectus roratus solomonensis).

Abstract: Squamous cell carcinoma of the infraorbital sinus was diagnosed in a 5-year-old Solomon Island eclectus parrot (Eclectus roratus solomonensis) that presented with exophthalmos of the right globe and an ulcerative mass of 2-months duration at the right commissure of the beak. The mass was 2.5 x 2 x 2 cm and contained caseous exudate. The ulcerative lesion was surgically debulked, but the bird died and was submitted for necropsy. Histopathologic examination of the infraorbital sinus revealed squamous cell carcinoma with no evidence of metastasis. The trachea was heavily infiltrated with thick, septate fungal hyphae, and evidence of fungal angioinvasion was observed in the trachea and muscular layer of the crop.

Key words: squamous cell carcinoma, infraorbital sinus, fungal, avian, eclectus parrot, Eclectus roratus solomonensis

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Clinical Report

A 5-year-old female Solomon Island eclectus parrot (Eclectus roratus solomonensis) was referred to the Louisiana State University Veterinary Medical Teaching Hospital (LSU-VMTH) for unilateral facial swelling involving the right eye and an ulcerative lesion containing caseous material at the level of the right commissure of the beak. The owner reported the facial swelling had increased during the previous 2 months. The bird's diet consisted of commercial pellets and mixed seeds with occasional fruits and vegetables. No diagnostic tests had been performed by the referring veterinarian. The bird had been empirically treated with cephalexin (100 mg/kg PO q8h) and nystatin (300 000 IU/kg PO q12h) for a presumptive upper-respiratory infection. According to the owner,

previous debridement of the lesion and application of a combined topical antibiotic /corticosteroid/anesthetic (neomycin sulfate/ isoflupredone acetate/tetracaine ointment applied q12h; Tritop, Pharmacia and Upjohn Co, Kalamazoo, MI, USA) had not been effective.

On physical examination, the bird weighed 400 g (subjective body score = 2/5) and was dehydrated. Signs of respiratory distress, such as intermittent open-mouthed breathing and head shaking, were exhibited, but no nasal discharge was observed. The bird had severe right periorbital swelling and exophthalmos and an irregular, ulcerative, necrotic lesion (2.5 X 2 X 2 cm) with caseous contents involving the right commissure of the beak (Fig 1). Shortened, blunt choanal papillae were also observed. All other physical examination findings were within reference range. Absence of fluorescein stain uptake in the right eye ruled out corneal ulceration.

[FIGURE 1 OMITTED]

The bird was admitted to the hospital, and a blood sample was collected and submitted for a complete blood cell (CBC) count and plasma biochemical analysis. A sample of the caseous material in the ulcerative lesion was sampled for bacterial culture and sensitivity, and survey radiographs were performed of the whole body and skull.

Initial empirical treatment included enrofloxacin (15 mg/kg PO q12h; Baytril, Bayer, Shawnee Mission, KS, USA) and carprofen (2 mg/kg PO q12h, compounded by the LSU-VMTH pharmacy into a 10 mg/ml suspension; Rimadyl, Pfizer Animal Health, New York, NY, USA). The bird was given 1 injection of vitamin A and [D.sub.3] (0.67 ml/kg IM; compounded injectable solution of vitamin A [1 x 105 IU/ml] and vitamin [D.sub.3] [1 x [10.sup.4] IU/ml], Veterinary Medical RX, Houston, TX, USA). Lactated Ringer's solution was administered for fluid replacement and maintenance (100 ml/kg per day plus 5% deficit corrected subcutaneously over 72 hours). Enteral support was initiated to provide maintenance plus additional calories at 66 Kcal/day (16 ml via gavage tube q12h; Emeraid Critical Care, Lafeber Co, Cornell, IL, USA).

Results of the CBC and plasma biochemical analysis were unremarkable with the exception of a mild anemia (packed cell volume [PCV] 40%; reference range, 45%-55%). (1) Whole-body radiographs were unremarkable. Skull radiographs revealed exophthalmos of the right globe and increased soft tissue surrounding the right orbit (Fig 2). Bone loss involving the right caudolateral maxilla, right jugal (zygomatic) arch, and right suborbital arch was suggested on the ventrodorsal projection, and sclerotic bone, at the level of the right caudolateral beak on both projections, was consistent with sequestration.

[FIGURE 2 OMITTED]

The differential diagnoses included infectious disease (mycobacteriosis, fungal or bacterial granuloma, poxvirus), hypovitaminosis A-induced abscess or granuloma involving the infraorbital sinus, foreign body reaction, trauma, and infiltrative neoplasia. Further diagnostic and therapeutic options discussed with the owner included debridement and biopsy of the abnormal tissue or palliative medical treatment. Two days after the bird's presentation, the owner opted for wound debridement.

Anesthesia was induced by face mask with 5% isoflurane and maintained with 2% isoflurane. The surgical area was prepped, and the necrotic wound was resected by radiosurgery (Surgitron, Ellman International Inc, Hewlett, NY, USA). Caseous material had invaded the retrobulbar space of the right eye, the right commissure of the beak, and the preorbital diverticulum of the infraorbital sinus and a large cavity remained after debridement (Fig 3). The bird recovered uneventfully from surgery.

[FIGURE 3 OMITTED]

Impression smears were made of the caseous material, which was also submitted for aerobic bacterial and fungal culture and sensitivity testing; samples for culture were plated on blood agar/MacConkey's media and inhibitory mold agar (PML Microbiologicals, Tualatin, OR, USA), respectively. Zeihl-Neelsen stain of the impression smears were acid-fast negative. No growth was noted on fungal culture, but bacterial culture revealed a heavy growth of Klebsiella pneumoniae, Staphylococcus species (coagulase negative), and Streptococcus species ([alpha]-hemolytic), all of which were resistant to enrofloxacin.

Enrofloxacin was replaced with amikacin sulfate (15 mg/kg IM q12h), ticarcillin disodium/clavulanate potassium (200 mg/kg IM q12h; Timentin, GlaxoSmithKline, Research Triangle Park, NC, USA), and metronidazole (50 mg/kg PO q12h; compounded by LSU-VMTH into a 50 mg/ml suspension). Pain management and fluid therapy were continued. The cavitated area involving the right side of the face was cleansed and debrided daily with 0.9% saline solution then packed with gauze, impregnated with a solution potentiating the activity of the broad-spectrum antimicrobials (Tricide, Molecular Therapeutics LLC, Athens, GA, USA). After 3 days of treatment, the bird lost weight and became anorectic. Despite gavage feeding, the bird did not improve and died 5 days after presentation. A necropsy was done at the owner's request.

On gross examination, a 1.5 x 1 x 0.5-cm cavitation extended from the right commissure of the beak to the caudoventral margin of the right orbit, at the level of the infraorbital sinus. A plug of tan, caseous material covered the caudal half of the cavity. The middle third of the trachea contained brown gelatinous material that conformed to the shape of the tracheal lumen. No other significant gross lesions were observed. Sections of periorbital tissue, infraorbital sinus epithelium, trachea, lung, crop, kidney, and liver were fixed in 10% neutral buffered formalin, processed routinely, and sectioned at 5 [micro]m. All sections were stained with hematoxylin and eosin for right microscopy.

Multifocal tubular mineralization was observed throughout the renal parenchyma. No abnormalities were observed in tissue from the brain, heart, spleen, liver, pancreas, and gastrointestinal tract. The right infraorbital sinus contained a densely eosinophilic coagulum of inflammatory cells, sloughed epithelial cells, and necrotic debris (Fig 4). The sinus epithelium was denuded, and the submucosa surrounding the affected sinus was thickened with dense collagen fibers and infiltrated with moderate numbers of foamy macrophages and fewer numbers of lymphocytes and plasma cells. Scattered islands of neoplastic squamous epithelial cells were observed within the collagen stroma (Fig 5a), and eosinophilic material consistent with early keratin pearl formation was evident at some of the neoplastic foci (Fig 5b). Neoplastic cells, with large nuclei and prominent nucleoli, exhibited mild anisokaryosis. The histologic diagnosis was squamous cell carcinoma of the infraorbital sinus.

[FIGURES 4-5 OMITTED]

Sections of the trachea contained widespread mucosal sloughing. The remaining tracheal submucosa and muscularis were heavily infiltrated with thick septate fungal hyphae. Aggregates of pale eosinophilic material mixed with septate fungal hyphae, sloughed tracheal epithelial cells, and debris were seen in the tracheal lumen (Fig 6). The lumen of the 2 primary bronchi contained mixtures of red blood cells (RBCs), sloughed pseudostratified ciliated epithelium, variable numbers of goblet cells, dense eosinophilic material, and scattered bacteria. Some of the secondary bronchi contained small aggregates of foamy macrophages. The crop lumen contained a thick layer of fibrin, degenerate leukocytes, and debris; scattered bacteria overlaid the serosal surface of the crop. Numerous vessels within the adjacent muscularis were filled with fungal hyphae; in the most severely affected vessels, vascular walls were necrotic and fungi extended through the mural remnants. Hyphae and mixed mononuclear inflammatory cells were found throughout the musculature of the crop, both between and within myofibers and muscle bundles. The histologic diagnosis was fungal tracheitis and fungal ingluvitis.

[FIGURE 6 OMITTED]

Discussion

Neoplastic disease in avian species is the subject of growing interest for veterinary practitioners both because of the increased clinical ability to diagnose avian neoplasia and because of the improved treatment options. As with mammals, many avian species develop spontaneous neoplasms, and the incidence, biological behavior, and morphologic types of neoplasia, as well as the numbers of organs affected, tend to increase as the animal ages. Neoplasia has been most commonly reported in Psittaciformes, especially budgerigars (Melopsittacus undulatus). (2,3)

Squamous cell carcinoma is a rare occurrence in birds of the order Psittaciformes; it accounts for 1.7% of the tumors examined in pet birds. (2-4) This type of tumor is observed most frequently in budgerigars, but no species, breed, or sex predilection has been documented in birds. Squamous cell carcinoma has been reported in a yellow-naped Amazon parrot (Amazona ochrocephala auropalliata), (5) a scarlet macaw (Ara macao), (2,4,6) an umbrella cockatoo (Cacatua alba), (2,7,8) a salmon-crested cockatoo (Cacatua moluccensis), (3) a peach-faced lovebird (Agapornis roseicollis), (2,7,9) Buffon's macaw (Ara ambigua), (10) a military macaw (Ara militaris), (2) a cockatiel (Nymphicus hollandicus), (2,4,6,8,9,11) a conure (Aratinga species), (2) and an elegant grass parakeet (Neophema elegans elegans). (9,11) Anatomic locations of squamous cell carcinoma described in captive and free-ranging birds include the tongue, pharynx, gastrointestinal system, uropygial gland, and upper beak as well as the skin of the head, eyelids, neck, chest, wings, and legs. (5-8,10,12-14) Although neoplasia, in general, appears to be uncommon in the eclectus parrot, squamous cell carcinoma affecting the globe and orbit has been previously reported. (15)

In most domestic species, squamous cell carcinoma is highly invasive but slow to metastasize, (16) and the same appears to be true for avian species. (13) As in the case described here, squamous cell carcinoma tends to be very vascular, and many tumors have ulcerated surfaces. (7,14) Another characteristic feature of this form of neoplasia includes infiltrative cords of moderately undifferentiated to poorly differentiated squamous cells that frequently form central cores of laminated keratin (keratin pearls), as seen in the infraorbital sinus of this bird. (8,14)

The avian infraorbital sinus is located ventromedial to the orbit and comprises numerous diverticula. Walls of the infraorbital sinus are composed almost entirely of soft tissue. Avian infraorbital sinusitis often manifests as swelling and erythema involving the periorbital area and nares, respectively. Chronic infections frequently cause inflammation and resultant swelling, particularly in cockatiels and Amazon and African grey parrots. Predisposing factors are primarily bacterial and nutritional; fungal and viral causes are less common. (17) The infraorbital sinus is reportedly seldom affected by squamous cell carcinoma based on the paucity of reported cases involving this location. (8,19) Severe deformities of the beak, cere, and preorbital diverticulum of the infraorbital sinus can also result from genetic anomalies, trauma, and infection.

In pet birds, the sinuses extend into the upper beak and are connected by a transverse canal lined rostrally by stratified squamous epithelium and caudally by alternating rows of ciliated ceils and intraepithelial mucous glands. (20) The infraorbital sinus frequently distends with mucus when its outflow tract is obstructed. We believe that the cause of intraorbital sinus distention in this parrot was attributed to squamous metaplasia of the respiratory epithelium secondary to vitamin A deficiency. Hypovitaminosis A was suggested by the blunted choanal papilla and the keratin accumulation within the turbinates. As a result, the mucociliary action of the respiratory epithelium was eliminated, ultimately impairing clearance and increasing the likelihood of upper respiratory infection with fungal organisms. Another likely cause of the distention was edema secondary to either lymphatic obstruction or vasodilation in the periocular region. Other common obstructive respiratory conditions in caged birds include granulomatous disease and congenital malformations. In this case, the squamous cell carcinoma possibly originated in an area of squamous metaplasia, or it may have developed in the region of the infraorbital sinus lined by stratified squamous epithelium.

To our knowledge, this is the first report of squamous cell carcinoma of the infraorbital sinus in an eclectus parrot. It is important to differentiate squamous cell carcinoma from other types of neoplasia affecting the infraorbital sinus that also carry a poor prognosis, such as papilloma, adenocarcinoma, fibrosarcoma, liposarcoma, and lymphosarcoma. (6,21-24) Because of the locally invasive nature of squamous cell carcinoma and its poor prognosis, some references do not suggest any course of action other than immediate euthanasia, perhaps, because many individuals are presented with fairly advanced disease. (6) Advanced imaging techniques, including ophthalmic ultrasonographic examination, magnetic resonance imaging (MRI), and computed tomography (CT), might have provided additional diagnostic information in our case. However, because of the bird's guarded prognosis, these diagnostic tests would have been of little practical use in helping to formulate a treatment plan and would have added significant additional expense.

Although no fungal organisms were observed in the sinus exudates, inhalation of fungal material from the necrotic site was the most likely cause of the fungal infection in the trachea. The crop may have become infected by the extension of fungal organisms from the trachea because the ingluvitis appeared to have originated from the serosal surface adjacent to the affected trachea. Tissue samples from the trachea and crop were not submitted for fungal culture, so definitive identification of the fungal organisms was not possible. Aspergillus fumigatus is the most frequently isolated fungal pathogen in birds, (25-27) and the septate branching morphology of the hyphae seen in this case was consistent with Aspergillus species. Infections with various species of Aspergillus occur in the upper and lower respiratory tract, trachea, air sacs, and lungs. (25-27) This saprophytic fungus is capable of penetrating vasculature and spreading to distant sites, including the central nervous system. Hyphal fragments possibly formed an embolus that lodged in a major organ system, thus resulting in death of this parrot. Although infraorbital distention and periorbital soft tissue swelling are most commonly associated with aspergillosis, culture of the caseous material in situ did not reveal the presence of fungal elements. Inability to culture fungus in this case was likely due either to an inappropriate environment for optimal growth or previous antifungal treatment by the referring veterinarian.

Combined antibiotic therapy of an aminoglyco-side and a [beta]-lactam has been used to treat life-threatening infections caused by gram-negative bacterial organisms and was chosen for this bird before reaching a definitive diagnosis. Two bactericidal drugs, used concurrently, can decrease the emergence of resistant organisms by additive or synergistic mechanisms. (28) Such therapy may be important in immunosuppressed avian patients harboring resistant bacteria or infections with multiple organisms. (28) In addition, the [beta-lactam antibiotic was chosen because it can be effective in an area of low-oxygen tension and in a possible anaerobic infection.

Treatment of neoplasia involving the head often involves tissue resection or dehulking; however, tumor control in avian medicine is still in its infancy. Therapeutic options that have been suggested or attempted include cryotherapy, chemotherapy, radiation therapy, radioactive implants, and photodynamic therapy. (29) In one study, surgical incision and immediate application of topical 5-fluorouracil once daily in 4 raptors with cutaneous squamous cell carcinoma proved to be curative with no recurrence for more than 2 years. (29) Radiotherapy was administered 2-3 weeks after surgery to treat squamous cell carcinoma of the mandibular beak in a Buffon's macaw without success; failure was attributed to radiation dosimetry or radioresistance. (10,29,30) Radiation with strontium-90 (Sr-90) has shown excellent results, leading to long-term remission with minimal complications in humans, dogs, cats, and avian patients. (31) However, we do not believe that radiation treatment with Sr-90 would have been efficacious in this case because of the tumor location. Treatment with Sr-90 has been reserved for shallow lesions, and in previously reported cases of squamous cell carcinoma successfully treated with Sr-90, surgical debulking was indicated before Sr-90 plesiotherapy. Photodynamic therapy was used to treat squamous cell carcinoma in the casque of a great hornbill (Buceros bicornis) on 2 occasions at 8-week intervals. (32) Histologically evident tumor-tissue necrosis was observed immediately after each treatment; however, tumor growth eventually resumed, even after aggressive surgical debulking was performed during the second treatment. In a second hornbill, surgery alone failed to control the carcinoma. (33)

In the case reported here, squamous cell carcinoma did not involve the sites most commonly affected by this form of neoplasia in pet birds, ie, tongue, pharynx, gastrointestinal system, uropygial gland, and upper beak, as well as the skin of the head, eyelids, neck, chest, wings, and legs. (5-8,10,12-14) Although local infiltration of the surrounding tissue is common with squamous cell carcinoma, in this parrot, it was difficult to reach a diagnosis because of the abscess overlying the tumor.

References

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From the Affiliated Veterinary Specialists, 9905 South US Hwy 17-92, Maitland, FL 32751, USA (Diaz-Figueroa); the Department of Veterinary Clinical Sciences (Tully) and the Department of Pathobiological Sciences (Evans), School of Veterinary Medicine, Louisiana State University, Skip Bertman Drive, Baton Rouge, LA 70803, USA; and the Department of Veterinary Anatomy and Radiology, College of Veterinary Medicine, University of Georgia, 501 DW Brooks Drive, Athens, GA 30602-7382, USA (Williams).
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Title Annotation:Clinical Reports
Author:Diaz-Figueroa, Orlando; Tully, Thomas N., Jr.; Williams, Jamie; Evans, Dawn
Publication:Journal of Avian Medicine and Surgery
Article Type:Case study
Geographic Code:1USA
Date:Jun 1, 2006
Words:3707
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