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Mucoepidermoid carcinoma in the skull of an orange-winged amazon parrot (amazona amazonica).

Abstract: A 33-year-old female intact orange-winged Amazon parrot (Amazona amazonica) presented for a slowly growing mass over the right eye. A computed tomography scan performed with and without intravenous contrast revealed a heterogeneous mixed soft tissue and mineraldense mass with a small area of non-contrast-enhancing fluid density located between the orbits at the caudal aspect of the nasal passages, with associated lysis of the right caudal nasal passage and the right frontal bone. Following euthanasia, the mass was found to consist of soft tissue between the right eye and nostril over the right frontal bone. Lysis of the underlying bone resulted in a bony defect leading into the infraorbital sinus along the dorsorostral aspect of the right eye. Histopathology revealed an unencapsulated, poorly demarcated, highly cellular neoplasm composed of islands and trabeculae of neoplastic cells embedded in abundant loose fibrovascular stroma which completely obliterated the cortical bone and sinuses of the rostral skull and infiltrated the surrounding muscle and soft tissue. Histologically, the tumor was consistent with a high-grade mucoepidermoid carcinoma, characterized by the presence of epidermoid, intermediate, and mucous-producing cell types. No evidence of metastasis was identified. The tissue of origin was suspected to be salivary or nasal mucous glands, but was difficult to confirm due to distortion of normal tissue architecture as a result of the tumor. Although mucoepidermoid carcinomas are a common salivary gland tumor in human medicine, they are not well recognized in avian species, and no specific case reports exist describing this pathology in an Amazon parrot. Despite the lack of distinct salivary glands in most avian species, mucoepidermoid carcinomas can occur, can cause significant clinical disease, and should be included as a differential diagnosis for avian patients presenting with similar lesions.

Key words: mucoepidermoid carcinoma, neoplasia, avian, psittacine bird, orange-winged Amazon parrot. Amazona amazonica

Clinical Report

A 33-year-old female intact orange-winged Amazon parrot (Amazona amazonica) presented on referral to the Kansas State University Veterinary Health Center (KSU VHC) for a chronic growing mass over the right eye. The parrot had a history of suspected Mycobacterium infection, treated 9 years previously, and had been reportedly healthy since completion of treatment. The mass over the right eye, first observed approximately 4 months prior, had been noted by the owner to be gradually increasing in size. The referring veterinarian had performed a fine-needle aspirate of the mass approximately 2 weeks prior to presentation. An aerobic culture of the aspirated material was reported to be negative. The referring veterinarian prescribed a 10-day course of enrofloxacin at 10 mg/kg, diluted and administered intramuscularly twice daily. The owner reported that despite removal of a large amount of fluid from the mass during the fine-needle aspirate procedure, the mass had returned to its original size within 3 days. When no improvement was noted following antibiotic therapy, the parrot was referred to the KSU VHC.

On presentation to the KSU VHC, the parrot was quiet, alert, and responsive. The patient was in good body condition (body condition score 3 out of 5) with a weight of 326 g. The right eye was moderately exophthalmic and ventrally rotated within the orbit. Epiphora and elevation of the right third eyelid was also noted. Retropulsion of the globe was not possible bilaterally. A generalized swelling of the dorsal skull and interorbital space was appreciated visually. On palpation of the region, a firm, approximately 0.5-cm-diameter round mass was present at the dorsorostral aspect of the skull between the orbits, with a softer, more fluid-filled defect present caudal to the mass above the right eye.

The parrot was anesthetized with isoflurane gas, induced via facemask and maintained via size 3mm uncuffed endotracheal tube. Blood was collected from the right jugular vein, using a 25-gauge needle attached to a heparinized 1 mL syringe, for complete blood count (CBC) and plasma biochemical profile. Pre- and postcontrast computed tomography (CT) was performed with a 16-slice helical scanner (GE Brightspeed, GE Health Systems, Waukesha, WI, USA), at 120 kV and 9 mAs and 0.625-mm slice thickness. The patient was positioned in sternal recumbency, and intravenous iohexol (515 mg/kg IV, Omnipaque 240 mg/mL injection, GE Healthcare Inc, Princeton, NJ, USA) was administered to obtain the postcontrast images. Following the CT scan, multiple fine-needle aspirates of the solid and fluid-filled portions of the periorbital mass were performed using 22-gauge needles. Approximately 1-2 mL of thick, dark reddish brown, viscous fluid was collected via the aspirates. Samples of the fluid were submitted for cytologic examination, acid-fast staining, and both aerobic and anaerobic cultures. A cloacal swab was also collected and submitted for acid-fast staining to screen for shedding of Mycobacterium organisms. Lactated Ringer's solution, supplemented with vitamin B complex (0.05 mL; Vitamin B Complex HP, Vet One, Boise, ID, USA), was administered subcutaneously. Anesthetic recovery was slightly prolonged but otherwise uneventful.

The CT scan revealed a heterogeneous mixed soft tissue and mineral-dense mass with a small area of non-contrast-enhancing fluid density located between the orbits at the caudal aspect of the nasal passages (Figs 1 and 2). At the point of largest diameter, the mass measured 16.03 mm deep X 14.54 mm wide X 12.21 mm long. This mass had associated lysis of the dorsal aspect of the right caudal nasal passage and the dorsal and lateral aspects of the right frontal bone. Differentials for this mixed lytic and proliferative mass associated with the caudal nasal passages and frontal bone included a chronic granulomatous lesion or neoplasia. Additional CT findings were consistent with mild focal aortic atherosclerosis and a right renal cyst, both of which were considered incidental. Cytologic examination of the aspirates from the mass showed macrophagic inflammation with abundant beaded rod-shaped bacteria, and degenerating epithelial cells. No acid-fast organisms were identified in the aspirate and cloacal swab samples. Aerobic and anaerobic cultures failed to grow any organisms.

The CBC showed evidence of a mild leukocytosis (total white blood cell count, 20 X [10.sup.3] cells/[micro]L; reference interval, 6-17 X [10.sup.3] cells/[micro]L) characterized by a heterophilia (heterophil differential 98%, absolute count 19.6 X [10.sup.3] cells/[micro]L; reference interval, 30%-80%) and lymphopenia (lymphocyte differential, 0%, absolute count, 0/[micro]L; reference interval, 20%-65%), in addition to mild anemia (packed cell volume 39%; reference interval, 40%-55%). (1) Plasma biochemistry revealed hypokalemia (2.4 mEq/L; reference interval, 3-4.5 mEq/L), elevated aspartate transaminase (AST, 835 U/L; reference interval, 130-350 U/L), alkaline phosphatase (ALP, 257 U/L; reference interval, 15-150 U/L), and creatine kinase (CK, 4105 U/L; reference interval, 45-265 U/L). (1) The leukocytosis, heterophilia, and lymphopenia were attributed to a stress leukogram in conjunction with active inflammation and infection within the mass. Hypokalemia was suspected to be related to a decline in appetite. Elevation of AST, ALP, and CK were suspected to be secondary to the necrosis and osteolysis associated with the rostral skull lesion.

Because of the poor prognosis associated with the invasive nature of the parrot's mass in conjunction with a declining clinical status, the owners elected euthanasia. Immediately following euthanasia, fine-needle aspirates of the fluid-filled portion of the mass were performed and the fluid placed into respective culturettes for both aerobic and anaerobic culture. On postmortem examination, the tissue between the right eye and nostril over the right frontal bone was soft and easily depressed. The underlying bone was found to be absent, with a 2- X 0.5-cm bony defect leading into the infraorbital sinus along the dorsorostral aspect of the right eye (Fig 3 A). Multiple small (2-3 mm X 1 mm) irregular fragments of bone were present within the sinus cavity. A slight concavity of the right frontal bone was present, leading to mild compression of the underlying frontal region of the brain.

Tissue samples were fixed in 10% buffered formalin, followed by decalcification with Cal-Ex Decalcifier solution (Fisher Scientific, Waltham, MA, USA) for 3 days. Samples were then processed routinely and stained with hematoxylin and eosin, in addition to acid mucicarmine and toluidine blue stains to demonstrate mucin production. Immunohistochemical staining for cytokeratin antibody was also performed. Within the rostral portion of the skull, an unencapsulated, poorly demarcated, highly cellular neoplasm completely obliterated the cortical bone of the skull and infiltrated the surrounding muscle and soft tissue (Fig 3B). The neoplasm was composed of islands and trabeculae of neoplastic cells embedded in abundant loose fibrovascular stroma. Approximately 70% of the cells were of intermediate type, 25% were mucous-producing cells, and 5% were epidermoid type cells. Active bone resorption was evident based on the scalloped edges of the little remaining trabecular bone and the presence of occasional osteoclasts within Howship's lacunae.

The predominant population of neoplastic cells were polygonal with distinct cell borders, a moderate amount of eosinophilic to amphophilic lacy cytoplasm, and an irregularly round to oval nucleus possessing vesiculate chromatin and 1-2 prominent nucleoli. Moderate anisocytosis and anisokaryosis were present, and 3 mitotic figures were seen in ten X400 fields. This cell type was intermediate between epidermoid and mucous-producing cells (Fig 3C).

The mucous-producing neoplastic cells formed acinar structures containing swollen cells with abundant clear cytoplasm and round central nuclei, or nuclei displaced to the periphery (signet-ring cells) (Fig 3D). Epidermoid cells were present individually or in nests, with abundant eosinophilic cytoplasm. Rarely, individual epidermoid cells possessed lamellar cytoplasmic keratinization or larger compact lamellations of keratin (keratin pearls). Frequent central cavitation with necrotic cell debris and proteinaceous and mucinous fluid was noted within islands of neoplastic cells. The presence of mucin in mucous-producing neoplastic cells and extracellularly within acinar lumina was confirmed with toluidine blue and acid mucicarmine histochemical stains (Fig 3E). Diffusely, neoplastic cells were positive for cytokeratin using histochemical staining (Fig 3F). In the periphery of the neoplasm, tubular structures were lined by cuboidal to columnar neoplastic cells, some of which possessed flattened basal nuclei and abundant clear vacuolated cytoplasm. The neoplasm was surrounded by fibrous stroma which contained poorly demarcated areas of granulomatous inflammation with cholesterol clefts, foamy macrophages, and few heterophils and multinucleated giant cells (xanthomas). Additional gross and histopathological findings included the presence of a pedunculated fibroma attached to the aorta via a vascular stalk within the coelom immediately cranial to the kidneys, as well as multifocal arterial atherosclerosis and mineralization.

Based on the histopathologic findings, a diagnosis of a high-grade mucoepidermoid carcinoma of the skull was made. The tissue of origin was difficult to determine because of the extensive invasion into the rostral skull and surrounding muscle and soft tissues. However, the neoplastic cell morphology and immunohistochemical staining properties were suggestive of a salivary or nasal cavity submucous gland origin.


In general, neoplasia in the order Psittaciformes is not common, with a prevalence of only 6.2% reported in one survey of 3545 cases. (2) Within the cases reported for Amazon parrots in the same survey, the most common tumors identified were squamous cell carcinomas, cloacal adenomatous polyps, cloacal papillomas, and biliary carcinomas. (2) The most common carcinoma reported in psittacine birds as a group is squamous cell carcinoma, which can occur anywhere on the body. (3)

When neoplasia is suspected, further diagnostic testing should be carried out to provide complete information about the lesion to guide treatment options and prognosis. Hematologic and biochemical analysis is necessary as a part of the minimum database of patient information. Diagnostic imaging such as radiography, ultrasonography, CT, or magnetic resonance imaging, with contrast as indicated based on the location of the lesion, provides valuable information regarding size, shape, and the specific anatomic location of the suspected neoplastic lesion. (4) In this case, a CT scan was performed in light of the location of the lesion within the delicate structures of the rostral cranium. This imaging modality provided detailed information about the involvement and lysis of the bones of the skull, which was supportive of a poor prognosis in this case.

Appropriate sample collection from the lesion itself is imperative for obtaining an accurate diagnosis. Sample collection can be performed via fine-needle aspirate, biopsy, or complete excision in cases where size and location allows. Surgical excision can double as both a diagnostic and treatment modality in some cases. (4) In this case, a fine-needle aspirate was elected, which unfortunately did not provide an antemortem diagnosis. Both core biopsy and surgical excision of the lesion were not considered possible due to the invasion of the surrounding osseous structures of the skull (notably, the frontal bone over the brain) observed on CT scan.

In the present case, the lesion was located within the osseous and soft tissues of the skull itself. Based on the clinical presentation and CT findings, the primary differential diagnoses for this case were neoplasia and granulomatous disease, such as mycobacteriosis, which had historically been treated in the patient several years prior to presentation. However, antemortem cytologic and acid-fast findings made a diagnosis of mycobacteriosis less likely, and neoplasia with secondary infection was considered the most likely cause of the condition.

Neoplastic differential diagnoses for this case included squamous cell carcinoma, nasal or sinus carcinoma/adenocarcinoma, lymphosarcoma, chondroma, fibrosarcoma, osteoma, and osteosarcoma, which have all been reported to affect the tissues of the rostral skull. (5,8) Histopathology following necropsy revealed a diagnosis of highgrade mucoepidermoid carcinoma of the skull, which has not been previously described in this species.

Mucoepidermoid carcinoma is well described in human medicine, where it is reported to be one of the most common malignant tumors of the salivary gland. (9-12) Histologically, this tumor is characterized by the presence of epidermoid, intermediate, and mucous-producing cells. (13) In some cases, immunohistochemical staining properties are required to distinguish mucoepidermoid carcinoma from squamous cell carcinoma or salivary adenocarcinoma. (13) In this case, the histological findings, presence of all 3 cell types, and the presence of mucin and cytokeratin confirmed the diagnosis of a mucoepidermoid carcinoma without the need for extensive immunohistochemical staining.

Although most commonly found in the major and minor salivary glands in humans, this tumor has also been reported in the nasopharyngeal tissues, the lung, and the bone of the mandible and maxilla, among other less common locations. (10,14-16) In veterinary medicine, spontaneous mucoepidermoid carcinomas have been reported in dogs and cats, an African lion (Panthera leo), and an African hedgehog (Atelerix albiventris), most commonly affecting the major salivary glands. (13,17-19) Mucoepidermoid carcinoma has been reported as a rare occurrence in birds. (3)

Due to the extent of tissue invasion and distortion of normal anatomy from the neoplasm described in this case, the tissue of origin was not definitively identified. Based on the properties of mucoepidermoid carcinoma as a well-described entity in other species, salivary tissue involvement was suspected, but origination from nasal mucous glands cannot be ruled out. Although most avian species do not have well-defined salivary glands, salivary tissue is often present within the oropharynx, notably within the maxillary, palatine, and sphenopterygoid regions. (8) The amount and distribution of salivary gland tissue is often dependent on the primary food preference of the species, but is typically present to some extent to provide lubrication during the swallowing process. (20) However, any disease affecting salivary tissue is exceedingly rare in avian species, and few reports exist of conditions affecting the mandibular salivary tissue. (8,21,22) Alternatively, the tumor may have originated from the mucociliary lining of the middle nasal concha, which is continuous with the nasal cavity itself. (23) In humans, mucoepidermoid carcinoma has been reported originating from the nasopharyngeal mucous glands. (10)

Mucoepidermoid carcinomas in humans are generally considered malignant but slow growing, exhibiting varying degrees of both local invasion and distant metastasis, depending on the grade of the individual tumor. (12) Each tumor is graded histologically as low, intermediate, or high grade, which typically correlates with the clinical behavior of the tumor and overall prognosis. (9,13) In the present case, local invasion with no evidence of metastasis had occurred, and the tumor was assigned a high grade histologically. It is possible that metastases may have developed further on in the disease course if the location of the tumor had been different, and the lesions not been identified as quickly.

In humans and domestic animals affected with mucoepidermoid carcinoma, treatment of choice is surgical excision, paired with radiation or chemotherapy. (9,12) Similar treatment strategies have been employed in veterinary medicine when treating salivary tumors in dogs and cats. (17) Although treatment for mucoepidermoid carcinomas has not been described in avian species, considerations for treatment remain the same as in other species. If possible, the tumor should be surgically excised, followed by adjunctive therapies as indicated by surgical margins or residual disease. Adjunctive chemotherapy or radiation therapy modalities have been reported in multiple avian species, but generally are based on extrapolated dosing regimens from companion animals. (4) Although euthanasia was elected in this case, surgery for complete excision of the affected tissues was not considered possible due to the extensive invasion into the frontal bone over the brain, and alternative therapies may have been recommended. Radiation therapy may be an option in future cases of mucoepidermoid carcinomas to attempt to slow the growth and local invasion of the tumor. If metastases also occur, then chemotherapy may be a more appropriate modality to consider in order to widely distribute the effects of the therapeutic agent.

This case describes a case of mucoepidermoid carcinoma affecting the osseous and soft tissue structures of the rostral skull of an orange-winged Amazon parrot. Although this tumor type is exceedingly rare in avian species based on the lack of reported cases, this and other types of salivary or mucous gland neoplasia should be considered in any bird with a similar clinical presentation.

Acknowledgments: We thank Dr Larry Snyder, who provided the initial evaluation of the case and clinical support as the patient's primary care veterinarian, as well as the staff and students of the Kansas State University Veterinary Health Center and Diagnostic Laboratory, who assisted with procedures and sample processing throughout the course of the case.


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Melissa R. Nau, DVM, James W. Carpenter, MS, DVM, Dipl ACZM, Denise Lin, MS, DVM, Sanjeev Narayanan, BVSc, MS, PhD, Dipl ACVM, Dipl ACVP, and Mackenzie Hallman, DVM

From the Department of Clinical Sciences, College of Veterinary Medicine. Kansas State University, 1800 Denison Ave. Manhattan. KS 66506, USA (Nau. Carpenter, Hallman); and the Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine. Kansas State University, K221 Mosier Hall. Manhattan, KS 66506. USA (Lin. Narayanan).

Caption: Figure 1. Mucoepidermoid carcinoma in an Amazon parrot. Midsagittal reformatted computed tomography image of the skull acquired at the level of the mass *. There is focal soft-tissue density swelling with granular mineral density throughout the mass. The patient is facing toward the left of the image (window 3000; level 700).

Caption: Figure 2. Mucoepidermoid carcinoma in the Amazon parrot in Figure 1. Transverse computed tomography image of the mass and rostral aspect of the brain acquired at the level of the eyes, showing multifocal areas of lysis of the right frontal bone *. The right side of the patient is on the left side of the image (window 300; level 35).

Caption: Figure 3. Mucoepidermoid carcinoma in the Amazon parrot in Figure 1. (A) On postmortem examination, the tumor tissue between the right eye and nostril over the right frontal bone was soft and easily depressed. A 2- X 0.5-cm bony defect leading into the infraorbital sinus along the dorsorostral aspect of the right eye was present (arrows). (B) The marrow and the air spaces of the entire rostral portion of the skull are diffusely infiltrated by an unencapsulated, poorly demarcated, highly cellular neoplasm composed of islands and trabeculae of polygonal neoplastic cells embedded in a loose fibrovascular stroma (solid arrows), with evidence of invasion into adjacent muscle tissue (open arrow) (hematoxylin and eosin; X0.5). (C) Neoplastic cells are polygonal with distinct cell borders, a moderate amount of eosinophilic to amphophilic lacy cytoplasm, and an irregularly round to oval nucleus with vesiculate chromatin and 12 prominent nucleoli, representing intermediate cells (open arrows). There is moderate anisocytosis and anisokarytosis, and 3 mitotic figures are seen in ten X400 fields. The preexisting trabecular bone is extensively lost; remaining trabeculae often have scalloped edges and occasional osteoclasts residing in Howship's lacunae indicating active bone resorption (solid arrow) (hematoxylin and eosin; X40). (D) Within islands of neoplastic cells there is frequent central cavitation with necrotic cell debris and proteinaceous and mucinous fluid. Rarely, there are individual neoplastic cells with lamellar cytoplasmic keratinization, representing epidermoid cells (arrow). Some islands form acinar structures containing swollen cells with abundant clear cytoplasm and round central nuclei or nuclei displaced to the periphery, representing mucous-producing cells (signet-ring cells; arrowhead) (hematoxylin and eosin; X24). (E) Mucin production by neoplastic cells was confirmed by toluidine blue (not shown) and acid mucicarmine histochemical stains (arrows) (acid mucicarmine stain; X20). (F) On immunohistochemical staining, the cytoplasm of the neoplastic cells was diffusely positive for cytokeratin (arrows) (pancytokeratin [AE1/AE3] immunohistochemical stain with red chromogen; X40).
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Title Annotation:Clinical Report
Author:Nau, Melissa R.; Carpenter, James W.; Lin, Denise; Narayanan, Sanjeev; Hallman, Mackenzie
Publication:Journal of Avian Medicine and Surgery
Date:Sep 1, 2017
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