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Mucocele in a spectacled owl (Pusilatrix perspicillata).

Abstract: A 6-year-old breeding female spectacled owl (Pusilatrix perspicillata) was presented for a soft, fluid-filled, spherical mass under the neck that had been increasing in size over the previous 3 days. Results of a fine-needle aspirate of the mass showed clear, pale-yellow fluid with a total protein of 12.6 g/L. Cytologic examination revealed erythrocytes, moderate numbers of heterophils, and numerous foamy mononuclear cells against a mucoid background. Macroscopically, the mass appeared to be attached firmly to the esophagus. The mass was excised surgically and submitted for histopathologic examination. The lesion comprised a circumscribed, fibrous-encapsulated multilocular cyst, lined by plump, goblet-type, cuboidal epithelial cells lying in abundant mucinous matrix. Findings were consistent with a mucocele of the esophageal mucosal gland. Excision was considered curative based on follow-up 6 months after initial presentation. To our knowledge, this is the first report of this condition in Strigiformes and indicates that mucocele should be included in the differential diagnosis of cervical masses in birds.

Key words: mucocele, sialocele, cervical mass, saliva, esophagus, avian, Strigiformes, spectacled owl, Pusilatrix perspicillata

Clinical Report

A 6-year-old female spectacled owl (Pusilatrix perspicillata) was presented for a soft tissue mass that had been enlarging for 3 days on the ventral aspect of the neck. The owl was part of a breeding pair from a private collection. Both birds were bred in captivity and kept in a large outdoor aviary with minimal human intervention and disturbance before each breeding season. The diet consisted of day-old chicks. The owner reported no previous medical problems.

On presentation, the owl was bright, alert, and responsive. The body weight was 600 g with a body condition score of 3/5. The bird was anesthetized by mask induction with 5% isoflurane for clinical examination to minimize stress induced by handling. Once anesthetized, the owl was intubated with a noncuffed endotracheal tube (3.0 mm) and maintained with isoflurane ranging from 1.5% to 3% concentration. A soft, fluid-filled mass was palpated on the ventral aspect of the neck, cranial to the thoracic inlet (Fig 1). The mass had a diameter of 7 cm, was easily moveable, and could be isolated from the underlying structures. A fine-needle aspirate of the mass produced 20 mL of clear yellow fluid. Fluid specific gravity analyzed by a refractometer was 1.010. The total nucleated cell count was 1.83 x [10.sup.3] cells/[micro]L, total protein was 1.26 g/dL, albumin was 0.46 g/dL, and fluid pH was 7.24. Cytologic examination showed erythrocytes, moderate numbers of heterophils, numerous foamy mononuclear cells, and occasional nonactivated macrophages. Some areas of amorphous background staining were consistent with mucus (Fig 2). A sample from the mass was submitted for aerobic and anaerobic culture, but no growth was obtained. These findings were suggestive of a mucocele.

The owl was anesthetized as described previously for surgical excision of the mass. An intravenous catheter was placed in the ulnar vein. Butorphanol (1 mg/kg IV; Torbugesic 1%, Fort Dodge Animal Health Ltd, Southampton, UK) and meloxicam (0.5 mg/kg IM; Metacam, Boehringer Ingelheim, Ingelheim/Rhein, Germany) were given for pain management. The owl was placed in lateral left recumbency, and the area was plucked and prepared aseptically. The skin was incised elliptically with minimal margin around the mass and the underlying structure was dissected bluntly. The trachea as well as the right jugular vein were displaced ventrally. A spherical, fluid-filled structure with a solid granular section attached to the esophagus was isolated. The esophagus was incised and the mass was resected with the surrounding esophageal tissue. The esophagus was closed in a continuous pattern and oversewn in an inverting pattern with a monofilament absorbable suture (Biosyn 3-0, Ethicon Inc, Edinburgh, UK). A Penrose drain was placed in the subcutaneous space, and the skin then was closed with single interrupted horizontal mattress sutures (Vicryl Rapide 3-0, Ethicon Inc). Recovery from anesthesia was uneventful. The owl was hospitalized for observation after surgery, and treatment was begun with meloxicam (0.5 mg/kg PO every 12 hours) and amoxicillin-clavulanate acid (125 mg/ kg PO every 12 hours. The drain and the catheter were removed 24 hours later, and the bird was discharged on the same medications to be continued for 1 week. The owner was instructed to feed only skinned, day-old chicks. The bird was comfortable eating and did not show any regurgitation. The wound healed without complication. and the bird was given whole prey 2 weeks after the surgery and tolerated the food well. No recurrence was observed in the 6-month postoperative period.

[FIGURE 1 OMITTED]

Histopathologic examination of the resected mass showed a fibrous-encapsulated, multilocular, cystic nodule lying within adipose tissue. The nodule comprised multiple, variably-sized cysts containing mucus-rich fluid with moderate numbers of macrophages and heterophils, proteinaceous debris, and red blood cells (Fig 3). Epithelia lining the spaces were plump cuboidal to columnar, with plentiful, slightly foamy, eosinophilic apical cytoplasm, often with goblet-type accumulations of mucus (Fig 4). Cells typically palisaded as a single layer with a distinct basement membrane, although clefts of subepithelial fluid extravasated in many areas. Cysts lay within a loose stroma rich in mucinous and proteinaceous floccular fluid, among which widely dispersed reactive fibroblasts and fibrocytes, and several bundles of smooth muscle fibers were present. In addition to the larger cystic spaces, smaller tubular/acinar structures, lined by similar populations of epithelial cells, were present. At the edge of the nodule, the interstitial collagen was variably compressed and formed a relatively distinct capsule in most areas. A narrow margin of excision was present in both sections examined with normal epithelial lining. Findings were consistent with a mucocele derived from the esophageal mucosal gland.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Discussion

In this report, we described a mucocele originating from the esophageal mucosal glands of an owl and its resolution by complete surgical excision of the cystic glandular tissue. Based on these findings, we recommend that mucocele should be considered as a differential diagnosis of cervical mass in strigiform birds.

Many birds lack clearly defined, organized, salivary glands as are found in mammals, and their size and significance vary with diet and feeding behavior. While some birds, such as woodpeckers, have well developed salivary glands, in most avian species the secretory tissue is more widely dispersed as simple glands. (1) Their distribution and concentration depend on the degree of keratinization of the tongue and oral cavity. Classification of the different glands can be confusing and difficult because the different glandular tissues merge with each other. Subepithelial, mucus-secreting glands extend along the esophagus under a stratified epithelium until the crop (although in some species, such as Strigiforrnes, a crop is absent). (2,3)

Salivary mucoceles, also termed sialoceles, occur when saliva leaks from the duct or directly from the gland. Leakage of saliva from the gland may incite an inflammatory reaction, granulation tissue formation, and fibrous encapsulation, (4) as was the case in this owl.

Mucocele has been described in a wide variety of species, including dogs, (5,6) cats, (5,6) ferrets, (7) horses, (8) and humans. (9,10) Clinical presentation in dogs and cats usually is as a painless swelling on the ventral aspect of the mandible or the ear canal. (5,6) In these species, lesions along the neck usually are associated with the submandibular glands. (5) Although pain was not assessed in the conscious owl before anesthesia, no obvious pain or difficulties in feeding behavior had been reported by the owners.

In dogs, the sublingual salivary gland is the gland in which mucoceles develop most commonly, but submandibular, parotid, and zygomatic mucoceles have been reported. (4,11) Location in the neck is common in dogs and has been described in humans as well. (5,12) In many species of birds, as mentioned above, the salivary tissue is not defined clearly and, thus, a salivary mucocele rarely can be related to a specific gland. Cases of esophageal mucocele have been described in humans undergoing a bypass esophagiectomy. (13)

Mucocele frequently is an idiopathic condition, but traumatic damage to the duct or gland may be recognized. Inflammation and calculus formation also are potential causes. (4,14,15) Spontaneous salivary mucoceles develop most commonly without a history of trauma or injury. (4) No history of trauma was reported in this owl, although this possibility cannot be excluded completely.

Salivary mucoceles are described rarely in birds, and more typically are oral, small, and multifocal, often secondary to hypovitaminosis A. (2) Vitamin A deficiency results in squamous metaplasia of the esophageal glands leading to secondary infections. (16-18) Sialocele has been reported in a yellow-naped Amazon parrot (Amazona ochrocephala auropalliata) associated with sialolith (a calculus of the salivary system). (19) Sialoliths have been reported in pigeons (Columba livia), and possible coinfection with herpes virus has been suggested. (2) There is a single report of sialolithiasis in a budgerigar (Melopsitticus undulatus). (16) Diet was reviewed and assessed as appropriate for the species. In this owl, no additional diagnostic tests were allowed by the owner, preventing further investigation for concurrent disease. Radiographs may have been useful to rule out sialoliths, which are radiodense. (19) Ultrasound may allow visualization of the vascularization of the mass. Computed tomodensitometry could have been used to assess the extension of the mass and delineate resection margins and was used successfully in cases of branchial cyst and thymoma. (20,21)

[FIGURE 4 OMITTED]

In this location, branchial cyst could have been a potential differential diagnosis. Branchial cysts are embryonic remnants of the pharyngeal arch and have been described in 2 Amazon parrots (Amazona species). (20) Both presented with a cervical, fluid-filled mass. In this owl, esophageal involvement, and the mucus-secreting epithelial lining and accumulating mucus are inconsistent with branchial cyst, although immunohistochemistry potentially could have been attempted to rule it out completely. Other differential diagnoses for a cervical mass are thyroid enlargement (goiter) or neoplasia. Goiter was common historically in budgerigars and cockatiels (Nymphicus hollandicus). (22-24) In raptors, thyroid adenocarcinoma has been reported in a wild barred owl (Strix varia) and a bald eagle (Haliaeetus leucocephalus). (21,23) Thymoma also was reported in a burrowing owl (Athene cunicularia). (25) Other possibilities are foreign body (eg, prey bone) perforation followed by abscessation. (2) Neoplasms, including carcinoma of the submucosal gland and papilloma, have been described in parrot species, (16) but, to our knowledge, not in raptors. Salivary cyst and concurrent adenoma have been described in humans, but there was no evidence to suggest neoplasia in this owl. (26)

Diagnosis of salivary mucocele relies on cytologic examination of a fine-needle aspirate supported by biopsy. Paracentesis and cytology of the mucocele typically yields a clear, yellowish, or blood-tinged mucoid fluid with low cellularity. A smear can be stained with a mucous-specific stain (periodic-acid Schiff) to confirm the presence of saliva. (11) As in this case, cytologic findings may be inconclusive, and definitive diagnosis is achieved by histopathologic examination.

Treatment for mucocele typically involves surgical excision. (4,11) Repeated aspiration associated with medical management is not recommended, because it can complicate further surgeries because of abscessation or fibrosis. (11) In dogs, complete sialectomy is necessary to solve cervical mucocele. (11) The salivary glands are isolated and the ducts followed to their origin. Ranulas can be marsupialized, but recurrence can appear as the wound closes. (11) A Penrose drain was used in the present case. In small mammals, inserting a drain for 1 to 3 days potentially will prevent seroma formation. (11) Overall, prognosis is excellent if the excision is complete. (11) Little information is available on esophageal surgery in birds. (27) The surgical approach of excising the gland was similar to that used with an esophageal perforation, with a standard closure using a simple continuous inverting pattern. (27) In dogs, dehiscence has been associated with continuous motion and longitudinal stretching. (11) Stricture as well as fistulization also are reported. (11) No complications were seen in this owl. Excision of part of the esophagus with a minimal margin prevented recurrence in the present case.

To regulate the production of saliva, medical management in humans has been suggested with anticholinergic drugs, with variable success. (10) In dogs, successful conservative treatment of an orbital mucocele using a sclerosing agent has been described. (28) The mucocele was aspirated while polidocanol 1% was injected into the gland. Polidocanol induces a fibrotic reaction, causing the lumen of the gland to occlude. (28) This technique might be useful in cases where surgical excision is not an option, but more cases are needed to assess the efficacy of the technique.

Acknowledgment: We thank Dr Geraldine Hale, Dechra Laboratories Leeds, for assistance with cytologic interpretation.

References

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Minh Huynh, DVM, MRCVS, Joao Brandao, LMV, Mikel Sabater, LVs, MRCVS, Mark F. Stidworthy, MRCVS, FRCPath, and Neil A. Forbes, FRCVS, Dipl ECZM (Avian)

From the Fregis Hospital Center, 43 Avenue Aristide Briand, 94110 Arcueil, France (Huynh); the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70808, USA (Brandao); the International Zoo Veterinary Group, Station House, Parkwood Street, Keighley, BD21 4NQ, UK (Stidworthy); and the Great Western Exotic Referrals, Shrivenham Road, Swindon, SN1 2NR, UK (Sabater, Forbes).
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Title Annotation:Clinical Reports
Author:Huynh, Minh; Brandao, Joao; Sabater, Mikel; Stidworthy, Mark F.; Forbes, Neil A.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2014
Words:2849
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