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Recurrent Subcutaneous Teratoma in an Adult Red-crowned Amazon Parrot (Amazona viridigenalis).

Abstract: An approximately 42-year-old, wild-caught, red-crowned Amazon parrot (Amazona viridigenalis) was evaluated for a subcutaneous mass to the right of the keel. Cytologic examination of a fine needle aspirate of the mass were suggestive of granulomatous inflammation. The mass was surgically excised, and the parrot was treated with oral nonsteroidal anti-inflammatory drugs. Histologically, the mass was diagnosed as a teratoma with stratified squamous epithelial and neuroectodermal components. Tumor cells extended to surgical margins. Two years later, the neoplasm recurred, with regrowth of only the neuroectodermal component. The neoplasm was again removed surgically, but it recurred again 14 months later, necessitating a third surgery. Histopathologic examination confirmed recurrence of the original neoplasm in both instances, with incomplete margins on both excisions.

Key words: subcutaneous mass, teratoma, tumor, avian, red-crowned Amazon parrot, Amazona viridigenalis

Clinical Report

An approximately 42-year-old, wild-caught, red-crowned Amazon (Amazona viridigenalis) parrot was presented to the University of Wisconsin-Madison, School of Veterinary Medicine, for evaluation of a subcutaneous mass to the right of the keel noted by the owner a few days before presentation. The bird, presumed male, was purchased as a young bird and owned by a single individual who reported that the parrot had been healthy for its entire life except for a respiratory infection when young. The diet consisted of variable commercial pellets, vegetables, fruit, and a small amount of human food items (<10%).

During the initial evaluation, the parrot was bright, alert, and responsive, and weighed 275 g. The bird was sedated with midazolam (2 mg/kg intranasally) for a thorough physical examination, which revealed no significant findings aside from a raised, firm, featherless mass (approximately 2 cm in diameter) on the right ventral thorax at the level of the mid-keel (Fig 1 A) that seemed to bother the parrot when palpated, despite sedation. Venipuncture for baseline blood parameters and fine-needle aspiration (FNA) of the mass were performed. Plasma biochemical analysis (avian/reptile biochemical profile; VetScan, Abaxis, Union City, CA, USA) revealed an increased creatinine kinase activity (1329 U/L; reference interval, 45-265 U/ L), mildly increased uric acid concentration (11.3 mg/dL; reference interval, 2-10 mg/dL), and mild hypophosphatemia (1.8 mg/dL; reference interval, 3.1-5.5 mg/dL). (1) Cytologic FNA demonstrated numerous keratinized, anucleate, squamous epithelial cells admixed with abundant eosinophilic, granular noncellular material. Embedded within the aggregates of squamous cells and debris were moderate numbers of poorly preserved and poorly dispersed nucleated cells, which were highly vacuolated and appeared bi- and multinucleated (interpreted as macrophage lineage). Some cells contained phagocytized debris including hematoidin. Cytologic interpretation was presumptive granulomatous inflammation with evidence of past hemorrhage. No definitive evidence of a neoplasm was found, nor were any microorganisms noted. Based on these results, surgical excision was the treatment of choice.

Two days after initial presentation, the bird was premedicated with midazolam (2 mg/kg IM) and butorphanol (1 mg/kg IM). After induction with isoflurane, the bird was intubated with a noncuffed, 3.0-mm endotracheal tube and maintained on isoflurane in 100% oxygen. The subcutaneous mass was excised routinely. The skin was closed with 5-0 monofilament synthetic absorbable suture (Maxon, Covidien Ltd., Minneapolis, MN, USA) in a simple interrupted pattern. Tissue glue was applied along the skin edges. During surgery, the bird received lactated Ringer's solution (50 mL/kg SC and 3.6 mL/kg IV) and 6% hydroxyethyl starch (11 mL/kg IV). Recovery was rapid and smooth. The bird was discharged the next day with meloxicam (0.55 mg/kg PO q24h) for 3 days in addition to an Elizabethan collar to prevent disruption of the surgical site.

The excised subcutaneous mass, measuring 2.1 x 1.7 X 1.5 cm, was submitted for histopathologic examination. On gross examination, the smooth, round nodule had an outer, variably firm, mottled light brown to black capsule that ranged from 1 to 7 mm thick. The center of the nodule contained 2 to 3 coalescing, brown to black foci as well as firm, caseous, tan-brown material that easily shelled out of a 1 cm diameter off-central cystic space (Fig IB). Histologically, the mass was nodular to cystic and partially encapsulated, and was comprised of two cellular populations: a multinodular, poorly delineated population of neuroectodermal cells (approximately 80% of the tissue), and variably-sized cysts and islands of squamous epithelial cells (approximately 20% of the tissue, not including cystic contents; Figs 2A, 2B).

The neuroectodermal cells were polygonal to spindle shaped, haphazardly arranged in short palisading bundles, streams, or disorganized poorly delineated aggregates, separated by a finely fibrillar, tangled, pale eosinophilic matrix reminiscent of neuropil. These cells had indistinct cell borders, a small-to-moderate amount of eosinophilic cytoplasm, a round-to-oval nucleus with vesicular-to-coarsely stippled chromatin, and 1-3 inconspicuous-to-large nucleoli. The mitotic index was two per 10 x 400 fields (2.37 [mm.sup.2]). On immunohistochemical staining, this population of cells positively labeled with neuron specific enolase (NSE) and neurofilament (including many positive fibrils in neuropil-like areas; Fig. 3A). These cells did not label with pancytokeratin, glial fibrillary acidic protein (GFAP), desmin, or smooth muscle actin. Vimentin, synaptophysin, and Factor VIII labeled few or no cells in psittacine control tissues or patient tissues and were deemed nondiagnostic.

The epithelial cells lined cysts in layers of keratinizing stratified squamous epithelium and formed small irregular islands and nests around the periphery of cysts, occasionally embedded within neuroectodermal tissue. No features of feather of follicular formation were present. The epithelial cells were positive for pancytokeratin (Fig. 3B), and negative for other markers (NSE, neurofilament, GFAP). With neural and epithelial components, the mass was diagnosed as a monophasic teratoma, with secondary heterophilic and granulomatous inflammation. Neoplastic cells of both types extended to surgical margins. Multiple sections of all tissues failed to show any additional cell types.

The bird was presented 12 days postoperatively for suture removal. At that time, it weighed 275 g and was bright, alert, and responsive. The incision was healed well and the sutures were removed.

Two years after initial presentation, the bird was again presented for evaluation of a mass on the ventrum, in the same location as the previously removed mass. On physical examination, the bird weighed 256 g. The only significant finding on physical examination was an ulcerative, actively-hemorrhaging mass, of approximately 2 cm in diameter, and an area of feather picking around the mass. Complete blood count and plasma biochemical profile revealed anemia (packed cell volume [PCV] 33%, reference interval, 40%-50% (1)), but no other clinically significant abnormalities.

Because of the continuous slow hemorrhage and anemia, in conjunction with the suspected discomfort to the bird and concern for possible regrowth of the original mass, surgical excision was elected for the same day. The bird was premedicated and anesthetized as described above. Lidocaine (6 mg/ kg) was used for infiltrative, local analgesia. A skin incision was made circumscribing the mass, which was removed. The skin was closed with 3-0 monofilament, nonabsorbable nylon suture (Ethilon; Ethicon US, Somerville, NJ, USA) in a simple interrupted pattern. During surgery, the bird received a balanced crystalloid solution (39 mL/ kg SC and 5.5 mL/kg IO) and one dose of meloxicam (1 mg/kg IM). The bird recovered rapidly and smoothly and was sent home the next day with an Elizabethan collar.

The ulcerative dermal mass, measuring 1.8 x 1.4 x 1.4 cm, was submitted for histopathologic examination. Histologically, a large central area of ulceration was superficial to a moderately well-delineated densely cellular mass. The mass consisted of dense sheets and interspersed intersecting bundles of spindle cells with indistinct cell boundaries, fibrillar eosinophilic cytoplasm, irregular ovoid nuclei with vesicular chromatin and prominent single or multiple nucleoli. The mitotic index was 17 per 10 X400 fields (2.37 [mm.sup.2]), and numbers of karyomegalic cells and multinucleated cells were increased compared to the initial biopsy. Multiple tissue differentiation was not evident, with only this spindle cell component. Results of immuno-histochemical staining for neurofilament and NSE were positive and similar to the labeling pattern of the neuroectodermal component of the original mass. Neoplastic cells failed to label for pancytokeratin and smooth muscle actin, and vimentin results remained nondiagnostic. Although the histopathologic results suggested a poorly differentiated spindle cell neoplasm on routine stains, immunohistochemical staining confirmed this to be consistent with regrowth of the neuroectodermal component of the original teratoma. Neoplastic cells extended to surgical margins.

The bird was presented 1 week afterwards for a recheck and suture removal. At that time, the bird weighed 250 g and was reportedly doing well at home. However, tissue glue remained in place over some of the sutures; therefore, removal of those sutures was postponed for another 17 days. At that time, the bird weighed 267 g and physical examination revealed no significant findings.

Follow-up phone conversation with the owner 13 months later revealed no concern and no apparent regrowth of the mass. However, 6 weeks later, the parrot was presented again for evaluation of recurrence of an ulcerative dermal mass at the previous site of removal almost 16 months previously. A full-body, contrast-enhanced computed tomography (CT) scan was performed to evaluate for signs of coelomic or lung metastases. The CT scan was performed with the bird under midazolam (2 mg/kg IM) and butorphanol (2 mg/ kg IM) sedation and reversed with flumazenil (0.05 mg/kg IM). Both lungs and coelomic cavity appeared within normal limits.

Surgical excision was performed as previously, except that larger skin margins were excised and the skin was closed using horizontal mattress sutures to help relieve tension at the incision site.

Histopathologic examination of the 1.8 X 1.5 X 1.2-cm mass showed a highly cellular population of spindle cells arranged in streams and whorls supported by a fine fibrovascular stroma that expanded and infiltrated the superficial and deep dermis. Neoplastic cells had indistinct cell borders with variable amounts of fibrillar eosinophilic cytoplasm, round-to-oval nuclei with finely stippled to vesiculated chromatin, and variably distinct nucleoli. Similar to the second biopsy, the mitotic index was 16 per 10 x400 fields (2.37 [mm.sup.2]), and numbers of karyomegalic and multinucleated cells were increased compared to the initial mass. Neuron specific enolase (NSE) and neurofilament immunohistochemical staining were performed, results of which showed evidence of a neuroectodermal population and intermediate filaments from neurons, respectively. Given the similarity to the previous biopsies, the neoplasm was considered consistent with recurrence of the neuroectodermal component of the previously diagnosed teratoma. Surgical margins once again were incomplete.

The wound was considered completely healed at re-evaluation 19 days postoperatively.


Teratomas typically are benign neoplasms of young animals occurring most commonly in the gonads. Benign mature teratomas are comprised of disorganized, multiple well-differentiated tissues derived from 1 or more of the 3 primary germ layers: ectoderm, mesoderm, and endoderm. (2-4) In this case, the mass was a mixture of well-differentiated neural and epithelial tissue, both of ectodermal origin, and multiple sections consistently failed to demonstrate any additional lineages. Although teratoma sometimes is defined as including tissues of 2 or 3 of the germ cell layers, neoplasms comprised of widely divergent tissues of one cell layer (as in this case with epidermal and neural tissue) conventionally qualify as teratomas but are more accurately termed 'monophasic teratomas.' Other terms for certain monophasic ectodermal teratomas, such as dermoid cyst or neuroectodermal tumor, do not fully reflect the combined epidermal and neuroectodermal nature of this case. Teratomas have been documented in mammals (including humans), chickens, other domestic poultry, a green iguana (Iguana iguana), and wild bird species. (5-22) Teratomas are rare in psittacine bird species, (23) and to our knowledge, no reports of subcutaneous teratoma in psittacine birds have been published.

Most teratomas in birds occur in either the ovary or testicle, but they also have been reported in the retroperitoneal, intracoelomic, anterior mediastinal, periorbital, and intracranial regions. (6,7,13-18,23) Because teratomas derive from abnormal or ectopic development of germinal cells from the primitive streak in the embryo, they generally are located in gonads or in tissues near the median axis during embryonic development. (17) To our knowledge, this is the first reported case of a subcutaneous teratoma in an avian species. Due to its location close to the keel, it is possible that this teratoma arose from remnant midline pluripotential germ cells.

The most frequently observed tissues in teratomas are connective tissues, cartilage, bone, skin, hair or feather, and neural tissues. (2-4) Cystic structures may contain keratin, as in this case, hair or feathers, or glandular secretory material. Granulomatous inflammation was noted cytologically and histologically and was mainly secondary to exposed keratin from a ruptured cyst. Few gram-positive cocci likely represented secondary infection with cutaneous flora.

Because the formation of teratomas is thought to result from abnormal or ectopic embryogenesis from germ cells, they may have existed since fetal life and often are first discovered in individuals at a young age. (2-4) In many cases, growth is very gradual over a long preclinical period during which the tumor may remain unnoticed. Discovery of the tumor may be incidental, or occur as a result of interruption of normal function because of encroachment on normal tissues. In many instances, teratomas continue slow and benign growth over a long period, with little change in histologic components. In other cases, the teratoma components may assume malignant qualities, including rapid growth, infiltration, and metastasis, as reported in an emu (Dromaius novaehollandiae), lesser kestrel (Falco naumanni), and a bald eagle (Haliaeetus leucocepha/us). (5,6,8) Teratomas are rarely discovered in adulthood. To our knowledge, only one other case of adult-onset teratoma has been reported in an avian species, which was a malignant transformation of a teratoma to teratocarcinomatosis in an emu. (5) It remains possible, however, for these teratomas to have existed in a state of slow growth with minimal benign effects until a point at which the tumor began to exhibit more profound effects on the patient. In our case, these effects appeared limited to discomfort.

Because of the benign nature of teratomas, surgical excision is the current treatment of choice (.20, 22) However, teratomas generally remain undetected until they impede normal organ function, resulting in clinical signs. By this point, size and location of the tumor may hinder complete surgical excision. (2,6,7,13-15,19 21) In human medicine, cases of malignant transformation of teratomas have been treated with chemotherapy in addition to surgical excision. (22) One case of surgical removal of a teratoma in an avian patient has been published, with the mass occurring periorbitally in a 6-week-old domestic turkey. (17) In that case, the bird survived surgery, but was lost to follow-up. Because teratomas tend to grow continually and harbor the risk of metastatic transformation, early surgical excision could prove beneficial to patient outcome. In this case, incomplete surgical removal resulted in tumor regrowth on two separate occasions. Both masses on regrowth were similar, with only the neuroectodermal component recurring, and with a similar increase in anaplastic features, including an increased mitotic index, increased anisokaryosis, and increased multinuclearity. Accurate diagnosis of the recurrent tumors would have been difficult without the first biopsy, and in the light of the poorly differentiated morphology, would have depended on immunohistochemical results indicating neuroectodermal origin (NSE and NF positivity).

Savannah Lauer, DVM, Marie E. Pinkerton, DVM, Dipl ACVP, Christoph Mans, Dr med vet, Dipl ACZM, Dipl ECZM (ZHM), and Grayson A. Doss, DVM, Dipl ACZM

From the School of Veterinary Medicine. University of Wisconsin-Madison, 2015 Linden Drive. Madison. WI 53706. USA.


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Caption: Figure 1. Subcutaneous teratoma in a red-crowned Amazon parrot. (A) The mass in situ, before first surgical excision. (B) The bisected mass after surgical excision, showing a cystic space filled with caseous material. Bar = 5 mm.

Caption: Figure 2. Photomicrographs of a subcutaneous teratoma in the Amazon parrot described in Figure 1. (A) The mass contains epithelial (*) and neuroectodermal (t) components, as well as adjacent heterophilic and granulomatous inflammation ([double dagger]); hematoxylin and eosin; bar = 100 [micro]m. (B) The mass has cystic epithelial (arrow) and neuroectodermal ([dagger]) components (hematoxylin and eosin, X20. Scale bar. 100 ([micro]m).

Caption: Figure 3. Photomicrographs of immunohistochemical stains of a teratoma in the Amazon parrot described in Figure 1. (A) Positive neurofilament labeling of neuroectodermal fibers (neurofilament immunohistochemical stain; bar = 100 nm). (B) Positive pancytokeratin labeling of epithelial components (y) adjacent to neuroectodermal component (t); pancytokeratin immunohistochemical stain; bar = 100 nm.
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Title Annotation:Clinical Reports
Author:Lauer, Savannah; Pinkerton, Marie E.; Mans, Christoph; Doss, Grayson A.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2019
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