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Branchial cyst with carcinoma in an umbrella cockatoo (Cacatua alba).

Abstract: A 16-year-old female umbrella cockatoo (Cacatua alba) was presented for a fluctuant, right-sided cervical mass that extended from the caudolateral edge of the right mandible to the coelomic inlet. Results of initial diagnostic tests were consistent with a cystic mass containing hemorrhage. Surgical exploration and removal of the mass was done, but because the hyoid apparatus was incorporated in the base of the cyst, complete surgical excision was not possible. Histopathologic results were consistent with a branchial cyst with carcinoma. Five months after surgery, the cockatoo exhibited intermittent periorbital swelling and epistaxis, and cytologic results of a fluid aspirate from the right infraorbital sinus were consistent with carcinoma. Results of magnetic resonance imaging revealed extensive abnormal T2 and short-tau inversion-recovery hyperintense tissue associated with the right side of the head and neck, infiltrating between muscle planes and extending into the right retro-orbital tissue and nasal cavity. At 7 months after surgery, the bird was severely dyspneic and was euthanatized. To our knowledge, this is the first report describing the diagnosis, management, and histologic characteristics associated with a branchial cyst with carcinoma in an animal.

Key words: branchial cyst, carcinoma, neoplasia, avian, umbrella cockatoo, Cacatua alba

Clinical Report

A 16-year-old female umbrella cockatoo (Cacatua alba) was presented for a right-sided cervical mass that was noticed a few days before examination. The patient had been owned for 14 years and had no previous medical problems. Physical examination revealed a fluctuant cervical mass that extended from the caudolateral edge of the right mandible to the coelomic inlet on the right side of the neck. The mass did not appear to cause the patient pain on palpation, and the cockatoo was able to swallow normally. The bird was in good body condition with a stable weight; the remainder of the physical examination was unremarkable. With an oral speculum in place, a red rubber catheter was passed through the mouth into the proximal esophagus and crop. The tube was palpated as separate from the mass, and no substances were obtained on aspiration. The initial diagnostic plan included a complete blood cell count (CBC) and plasma biochemical analysis, whole-body radiographs, and a fine-needle aspirate of the mass.

For the diagnostic procedures, anesthesia was induced and maintained with isoflurane in 100% oxygen. Results of the CBC showed a mild, regenerative anemia (packed cell volume [PCV], 35% with 1+ polychromasia; reference interval PCV, 40%-48%) and moderate to marked monocytosis (20%; reference interval 0%-1 %). (1) Results of the biochemical panel revealed an increased creatine kinase activity (359 U/L; reference interval, 95-305 U/L), mild hypoalbuminemia (1.2 g/dL; reference interval, 1.8-3.1 g/dL), and a decreased albumin: globulin ratio (0.6; reference interval, 2.0-4.5). (1) Results of radiographs revealed a bilobed, smoothly marginated, homogenous, right-sided soft tissue opacity that extended from the base of the skull to the coelomic inlet (Fig 1). The mass measured 9.9 X 3.7 cm, and the crop could be visualized separate from the mass.

An area over the middle of the mass was aseptically prepared, and the mass was aspirated; a clear to red-tinged fluid was obtained. On cytologic examination, the fluid was low in cellularity and had a light pink stippled background that contained moderate numbers of erythrocytes. Low to moderate numbers of vacuolated macrophages (including rare erythrophagocytic cells) were present, as well as dense sheets of tightly clustered epithelial cells with deeply basophilic cytoplasm and centrally placed round nuclei. The results were consistent with cystic fluid and hemorrhage.

The owner was offered advanced imaging (computed tomography [CT] or magnetic resonance imaging [MRI]) to further characterize the lesion; however, imaging was declined, and surgical exploration and removal of the mass was elected.

The patient was premedicated with butorphanol (2 mg/kg IM, Torbugesic, Ft Dodge Animal Health, Ft Dodge, IA, USA) and midazolam (0.3 mg/kg IM). Anesthesia was then induced with 2.5% isoflurane in 100% oxygen administered by face mask. The bird was intubated with an uncuffed endotracheal tube, and anesthesia was maintained with 1.5%-2.0% isoflurane for the duration of the procedure. An intraosseous catheter was inserted into the distal left ulna, and crystalloid fluids were administered (10 mL/kg per hour) throughout the procedure. The patient was placed in left lateral recumbency, and the region over the mass was plucked, aseptically prepared, and draped using sterile technique. An incision was made from the base of the right mandible to the coelomic inlet. The right cervicocephalic air sac was incised to facilitate removal of the cyst. The skin and subcutaneous tissues were gently dissected from the surface of the cyst. The esophagus, crop, jugular vein, and vagus and glossopharyngeal nerves were identified at the ventromedial aspect of the cyst and gently dissected from the cyst's surface. The caudal edge of the cyst was isolated from the surrounding structures and retracted cranially. The cranial edge of the cyst extended medially to the caudal edge of the right mandible. The jugular vein and the hyoid apparatus were incorporated in the base of the cyst. Two encircling ligatures (PDS II, Ethicon, Somerville, NJ, USA) were placed around the cyst just distal to these structures. The cyst was then transected distal to the sutures and as much of the cyst excised as possible. The area was flushed with saline and the skin was closed. Before recovery, the bird was given enrofloxacin (10 mg/kg IM; Baytril, Bayer Health Care, Shawnee, KS, USA), meloxicam (0.5 mg/kg IM, Metacam, Boehringer Ingelheim Vetmedica, St Joseph, MO, USA), and a second dose of butorphanol (1 mg/kg IM), and the intraosseous catheter was removed.

The cockatoo recovered uneventfully from anesthesia. Mild cervical subcutaneous emphysema was observed 4-6 hours after the procedure, but resolved without intervention. Meloxicam (0.5 mg/ kg PO q24h for 5 days) and enrofloxacin (10 mg/kg PO q12h for 7 days) were continued after surgery. The morning after surgery, the cockatoo appeared comfortable, was interactive and eating, and was discharged from the hospital.

Grossly, the cyst appeared cylindrical and thin-walled and contained 30-40 mL of serosanguinous fluid with suspended white flocculent material. The inside of the cyst was lined with adherent white nodular friable structures, which were most prominent cranially. Bacterial culture showed no growth after 7 days. Histopathologic examination revealed a cystic structure lined by simple to variably stratified cuboidal or columnar epithelial cells. Approximately 80% of the lining was disorganized and dysplastic, and in these areas, neoplastic cuboidal to polygonal cells formed variably thick papillary fronds with a fibrovascular core that extended into the lumen and formed islands within the lumen (Fig 2a). Neoplastic cells frequently contained variably vacuolated, eosinophilic cytoplasm and round to oval nuclei with finely stippled chromatin. There was moderate anisocytosis, anisokaryosis, and 5 mitotic figures per 10 X400-power fields. Multifocal islands and tapered cords of cuboidal cells were present within the submucosa. Neoplastic cells were focally present within a lymphatic vessel and extended to the surgical margins (Fig 2b). Aggregates of foamy macrophages with occasional golden brown granular material (hemosiderin) were present within the submucosa. The final diagnosis was branchial cyst with carcinoma, lymphatic invasion, and incomplete excision.

Radiation therapy was recommended for treatment of the remaining carcinoma; however, it was declined. The patient was rechecked every 2-4 weeks after surgery. For 4 months after surgery, incisional healing was good and no mass was palpable under the lateral edge of the mandible.

Five months after surgery, the cockatoo presented with intermittent right ventral periorbital swelling and an episode of epistaxis from the left nostril. Physical examination showed a moderate amount of fluctuant right periorbital swelling, but no mass was palpated under the lateral edge of the mandible. Results of blood tests revealed an improved mild monocytosis (4%), mild hypoalbuminemia (1.5 g/dL), and a decreased albumin: globulin ratio (0.7); however, the PCV (41%) was within the reference interval. (1) The creatine kinase activity was more elevated (1468 U/L) compared with the previous value.

The patient was anesthetized, similar to before, for whole-body radiographs (Eklin EDR6, Eklin Medical Systems, Carlsbad, CA, USA) and infraorbital sinus aspiration. The radiographs were unremarkable, with no mass regrowth noted. Bloodtinged fluid was aspirated from the right infraorbital sinus and submitted for cytologic evaluation.

On cytologic examination, the fluid appeared poorly cellular; however, a few moderately sized. tight clusters of epithelial cells were present in a moderately bloody background. The cells examined had a variable nuclear: cytoplasmic ratio with variably abundant pale blue cytoplasm and large round to irregularly round nuclei. The chromatin pattern was finely reticular to lacy, and occasional multiple nucleoli were seen. Anisocytosis and anisokaryosis were mild. Given the presence of features of malignancy and clinical history, carcinoma was considered likely.

Magnetic resonance imaging was performed to evaluate the extent of underlying disease. The study was performed using a 1.5T superconductive magnetic resonance system (Siemens Magnetom Espree, Erlangen, Germany). The patient was anesthetized and placed in dorsal recumbency, and the head and neck were wrapped in a small flex coil. Sequences acquired were sagittal T2-W spin echo (SE; time of repetition [TR] = 4253 milliseconds; time of echo [TE] = 111 milliseconds; slice thickness [SL] = 2 mm), transverse T2-W SE (TR = 3000 milliseconds; TE = 107 milliseconds; SL = 2 mm), transverse T1-W SE (TR = 311 milliseconds; TE = 12 milliseconds; SL = 2 mm), dorsal T1-W SE (TR = 465 milliseconds; TE = 12 milliseconds; SL = 3 mm), dorsal short-tau inversion-recovery sequence (TR = 6010 milliseconds; TE 32 milliseconds; time of inversion = 150 milliseconds]. Dorsal and transverse T1-W SE images were repeated after intravenous administration of 0.1 mL contrast medium (Magnevist, Bayer Healthcare Pharmaceuticals, Wayne, NJ, USA).

The MRI examination revealed extensive abnormal T2 and short-tau inversion-recovery hyperintense tissue associated with the right side of the head and neck, extending from an intermuscular location in the right cranial neck rostrally, infiltrating between muscle planes, and extending into the right retro-orbital tissue and nasal cavity. This abnormal tissue was slightly hyperintense on T1-weighted images and showed strong contrast enhancement (Fig 3).

Given the severity of disease and poor long-term prognosis, the owner decided not to pursue additional surgery, and radiation therapy was declined. Seven months after the initial surgical excision of the mass, the patient was presented for severe dyspnea, and euthanasia was performed.

At necropsy, disseminated white-tan, friable, round to irregular papillary nodules ranging from pinpoint to 9 X 5 X 2 mm were present within the cervical subcutis and coelomic inlet, and overlying the cervicocephalic air sacs, crop, and cranial pectoral muscles. Caudal to the right mandibular ramus was a white-tan, soft, friable, irregular, papillary mass (3.5 X 1.7 X 1.5 cm) that extended laterally along the ventrolateral bony orbit and caudal to the globe, replacing the retro-orbital tissue and filling the infraorbital and postorbital diverticula of the right infraorbital sinus (2 X 1.5 X 0.5 cm). Affected and routine tissues were collected into 10% buffered formalin. The tissue samples were routinely processed and paraffin embedded, and 4-5-[micro]m sections were prepared and stained with hematoxylin and eosin.

Microscopically, the masses in the coelomic inlet were composed of neoplastic polygonal cells that formed arborizing, papillary projections overlying a fibrovascular core that contained scattered lymphocytes and plasma cells. Neoplastic cells were occasionally ciliated and had variably distinct cellular borders, a moderate amount of lightly basophilic cytoplasm, and polygonal nuclei with vesicular to marginated chromatin. Anisocytosis and anisokaryosis were moderate, with 9 mitotic figures per 10 X400-power fields. Neoplastic polygonal cells, similar to those described in the coelomic inlet masses, multifocally expanded the cervicocephalic air sac epithelium and subcutis, and composed the mass distal to the right mandibular ramus. The abnormalities were consistent with a branchial cyst with carcinoma and cervicocephalic air sac, subcutaneous, and infraorbital sinus metastases.

Discussion

This report describes the diagnosis, management, and histologic characteristics associated with a branchial cyst with carcinoma in an umbrella cockatoo. To our knowledge, this is the first description of a branchial cyst with carcinoma in an animal.

Branchial cysts are rare congenital defects that are caused by a failure of the embryologic pharyngeal or branchial apparatus to form properly. During normal development, the chick embryo develops 5 pairs of pharyngeal arches. (2) The development of each arch is intricately coordinated to mature into important structures of the head and neck. Branchial defects can occur anywhere along these embryologic structures and can present clinically as cysts, sinuses, or fistulas. All are lined by epithelium; therefore, they are distinguished by their number of openings. Cysts have no external opening, sinuses have 1 opening, and fistulas have 2 openings. (3) They are classified into 4 types based on their embryologic arch origin, which has been described elsewhere. (3-6)

Branchial abnormalities have been documented in veterinary species, including Amazon parrots (Amazona species), dogs, cats, horses, and mice. (7-19) Branchial cysts seem to make up most of the cases reported, with only 1 case of a suspected branchial sinus documented in a foal. (11) As seen in the case reported here, branchial cysts appear more likely to present in mature animals, whereas fistulas and sinuses are typically diagnosed early in life. (7-9, 11, 15, 16)

Methods to differentiate a branchial cyst from other causes of cervical swelling include clinical presentation, anatomic location, radiographs, blood tests (hematologic testing and plasma biochemical analysis), cytologic evaluation of cyst contents, advanced imaging, and histopathology. (7,10)

The hematologic findings of a moderate monocytosis in this case were similar to those reported in an Amazon parrot. (7) In that report, histopathologic findings in the parrot were consistent with a branchial cyst with neoplasia (in situ carcinoma). Neoplasia has been reported to cause monocytosis and likely contributed to this finding in both cases. On histologic examination, macrophages were within the submucosa and lumen of the cysts of both birds, suggesting an increased tissue demand. Novel blood test results in this cockatoo were a mild, likely regenerative anemia, hypoproteinemia, and a low albumin: globulin ratio. These findings are consistent with blood loss, especially given the cytologic diagnosis of hemorrhage in the cystic fluid and improvement after cyst removal. The low albumin, however, could also be secondary to the laboratory detection technique; mammalian techniques for measuring albumin often give artificially lower values when used in birds. Ideally, plasma protein electrophoresis would have been performed to further characterize any changes in plasma proteins.

Preferably, advanced imaging (CT or MRI) would have been performed before surgical excision. In the human and veterinary literature, ultrasound, CT, and MRI have been described in the diagnostic workup of branchial cysts. Ultrasound can be used to evaluate extent and composition of the mass but is of limited value for determining origination and topographic anatomy. (7,9) Both CT and MRI can help determine origin and topographic anatomy, especially for surgical planning. One report suggests that MRI seems to be a better diagnostic tool when compared with CT in humans because of the greater contrast resolution and multiplanar imaging techniques. (4) In the veterinary literature, use of MRI to image branchial cysts has not been described. For this case, advanced imaging likely would have been beneficial before surgery, especially because the cyst appeared to incorporate the jugular vein and hyoid apparatus cranially. More aggressive surgical management may have been possible if the cranial-most extent of the lesion could have been identified before surgery, and imaging would have given the clinicians an idea of how much of the lesion remained for planning and prognosis purposes after surgery. Contrast-enhanced MRI performed after recurrence of clinical disease was consistent with the necropsy findings and depicted the extent of disease with great detail. For suspected cases of branchial cysts, MRI should be considered in the diagnostic work-up, especially if associated neoplasia is suspected.

Typically, on histopathologic examination, branchial cysts are lined by a single epithelial type or combination of epithelial types and are variably ciliated. (8,20) The initial histologic findings in this case were consistent with a branchial cyst but were unique in the diagnosis of carcinoma. The nonneoplasic portions of the branchial cyst in this cockatoo were similar to previous reports: specifically, a combination of nonciliated epithelial types, which made up approximately 20% of the cyst lining. The remainder of the lining (80%) was initially disorganized and dysplastic, progressing to epithelial neoplasia (carcinoma).

A complicating factor in the treatment and prognosis for the branchial cyst in this case was the presence of carcinoma within the cyst. Carcinoma in situ has been previously diagnosed within the wall of a branchial cyst in an Amazon parrot. (7) A diagnosis of carcinoma in situ means that the epithelium of the branchial cyst has been expanded by neoplastic cells that have not yet breached the basement membrane. The mass in our case did breach the basement membrane; it extended into the submucosa and metastasized to lymphatic vessels. Carcinoma in situ may represent a premalignant lesion that could develop into a branchial cyst with carcinoma. (7) In the human medical literature, carcinoma arising from branchial cysts is controversial. Many sources debate that previously diagnosed branchial cysts with carcinoma are actually cystic metastases from other primary tumors; however, few sources debate the rarity of occurrence of true branchial cyst carcinomas. (21) Criteria have been developed and later modified to diagnose branchial cyst carcinoma and include the anatomic location unique to branchial cysts, the histologic appearance, and the absence of a primary tumor elsewhere. (21) Commonly, primary tumors in the neck of humans arise from the tonsils, Waldeyer's ring (pharyngeal lymphoid tissue), or cervical lymph nodes, none of which are present in birds. (21,22) This case likely fits the criteria proposed: the location on the lateral neck extending from the submandibular area; the histologic appearance of normal branchial cyst epithelium progressing from dysplastic to neoplastic; and the absence of tumor elsewhere.

The treatment of choice for a branchial cyst, or branchial cyst with carcinoma in situ, is complete surgical removal. (5,7,21) When branchial cyst with carcinoma is diagnosed in human patients, wide surgical excision with postoperative radiation is recommended. (21) Unfortunately, no clinical reports describe treatment for branchial cyst with carcinoma in an animal. In the present case, complete surgical excision was deemed not possible because of the incorporation of the hyoid apparatus. Radiation therapy has been described in avian patients, (23-28) including a few patients with various types of carcinoma, (23,24) but treatment success is variable and often poor. (28)

The prognosis for patients with uncomplicated branchial cysts is good, as long as surgical complications are not severe. (8) All reported cases in animals describe no recurrence after surgical excision for cases with follow-up. (8-16) Reports of complicated branchial cysts (carcinoma in situ) in the veterinary literature also describe no recurrence with complete surgical excision. (7) Data on the prognosis for branchial cyst with carcinoma in humans is scarce, with few confirmed cases. In the confirmed case reports, most patients with complete surgical excision with or without radiation therapy had long-term survival. (21,29) The presence of carcinoma with incomplete surgical excision, as well as neoplastic cells within a lymphatic vessel, certainly contributed to the local invasion and metastasis in this case.

References

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(2.) Bellairs R, Osmond M. Gut, coelom, and respiratory system. In: Bellairs R, Osmond M, eds. The Atlas of Chick Development. San Diego, CA: Elsevier Academic Press; 2005:69-80.

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(21.) Jereczek-Fossa BA, Casadio C, Jassem J, et al. Branchiogenic carcinoma--conceptual or true clinico-pathological entity. Cancer Treat Rev. 2005;31 (2): 106-114.

(22.) King AS, McLelland J. Lymphatic system. In: King AS, McLelland J, eds. Birds: Their Structure and Function. Eastbourne, UK: Bailliere Tindall; 1984:229-236.

(23.) Pignon C, Azuma C, Mayer J. Radiation therapy of uropygial gland carcinoma in psittacine species. Proc Annu Conf Assoc Avian Vet. 2011:263.

(24.) Manucy TK, Bennett RA, Greenacre CB, et al. Squamous cell carcinoma of the mandibular beak in a Buffon's macaw (Ara ambigua). J Avian Med Surg. 1998; 12(3): 158-166.

(25.) Freeman KP, Hahn KA, Admas WH, et al. Radiation therapy for hemangiosarcoma in a budgerigar. J Avian Med Surg. 1999; 13(1):40-44.

(26.) Lamberski N, Theon AP. Concurrent irradiation and intratumoral chemotherapy with cisplatin for treatment of a fibrosarcoma in a blue and gold macaw (Ara ararauna). J Avian Med Surg. 2002; 16(3):234-238.

(27.) Filippich LJ. Tumor control in birds. Semin Avian Exot Pet Med. 2004; 13:25-43.

(28.) Barron HW, Roberts RE, Latimer KS, et al. Tolerance doses of cutaneous and mucosal tissues in ring-necked parakeets (Psittacula krameri) for external beam megavoltage radiation. J Avian Med Surg. 2009; 23(l):6-9.

(29.) Maturo SC, Michaelson PG, Faulkner JA. Primary branchiogenic carcinoma: the confusion continues. Am J Otolaryngol. 2007; 28(1):25-27.

Katherine Baine, DVM, Michelle Nobrega-Lee, DVM, Michael P. Jones, DVM, Dipl ABVP (Avian), James Steeil, DVM, Brynn McCleery, DVM, Edward Ramsay, DVM, Dipl ACZM, Juergen Schumacher, Dr Med Vet, Dipl ACZM, Dipl ECZM, Dipl ECZM (Herpetology), and Silke Hecht, Dr Med Vet, Dipl ACVR, Dipl ECVDI

From the Departments of Small Animal Clinical Sciences (Baine, Jones, Steeil, McCleery, Ramsay, Schumacher. Hecht) and Biomedical and Diagnostic Sciences (Nobrega-Lee). College of Veterinary Medicine, University of Tennessee, 2407 River Dr. Knoxville, TN 37996, USA.
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Title Annotation:Clinical Reports
Author:Baine, Katherine; Nobrega-Lee, Michelle; Jones, Michael P.; Steeil, James; McCleery, Brynn; Ramsay,
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Sep 1, 2014
Words:3975
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