Surgical removal of a thymoma in a burrowing owl (Athene cunicularia).
Article Type: Report
Subject: Thymoma (Diagnosis)
Thymoma (Care and treatment)
Burrowing owl (Diseases)
Burrowing owl (Care and treatment)
Veterinary surgery (Methods)
Authors: Kinney, Matthew E.
Hanley, Christopher S.
Trupkiewicz, John G.
Pub Date: 06/01/2012
Publication: Name: Journal of Avian Medicine and Surgery Publisher: Association of Avian Veterinarians Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2012 Association of Avian Veterinarians ISSN: 1082-6742
Issue: Date: June, 2012 Source Volume: 26 Source Issue: 2
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 298292704
Full Text: Abstract: A 12-year-old male burrowing owl (Athene cunicularia) was presented for evaluation of a mass in the right cervical region. A thymoma was diagnosed after surgical resection and histopathologic evaluation. Extensive adherence of the thymoma to the esophagus and suspected invasion into the right jugular vein contributed to a poor postsurgical outcome. Diagnosis and treatment of thymomas in avian species is similar to that in mammals. Surgical removal of noninvasive thymomas is usually curative. Thymomas are rarely reported in avian species and this is the first report in a strigiform bird.

Key words: thymoma, neoplasia, soft tissue surgery, avian, burrowing owl, Athene cunicularia

Clinical Report

A 12-year-old male burrowing owl (Athene cunicularia) presented to the veterinary hospital at the Toledo Zoo after keeper staff observed a swelling in the right cervical region. The bird had been healthy except for a period of lethargy and an abnormal posture 6 months earlier. At that time, a physical examination, complete blood cell count, serum biochemical profile, and whole body radiographs were performed. The only abnormal finding was a 1.5 x 1-cm swelling palpated in the cervical region. On radiographs, small bones appeared to be in the mass and it was considered to be a normal "pellet."

On current physical examination, a 3 x 3-cm firm, subcutaneous mass was present in the right cranial cervical region and was displacing the tongue dorsally. The trachea was palpable superficial to the mass. A metal gavage tube was easily passed into the esophagus, which was displaced to the left of midline. The bird had lost over 12% of its body weight over the 6 months, decreasing from 184 g to 162 g. No other abnormalities were observed on examination. The bird was returned to its exhibit after administration of subcutaneous fluids (10 mL Normosol-R, Hospira Inc, Lake Forest, IL, USA) with 0.5 mL of 50% dextrose. The bird was fasted overnight for anesthesia the next morning.

Anesthesia was induced with isoflurane administered by face mask. After intubation with a 1.5mm endotracheal tube, the bird was given butorphanol (1.3 mg/kg IM; Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) and maintained on isoflurane and oxygen for the duration of the procedure. Orthogonal view radiographs of the cervical region demonstrated a 3 x 3-cm soft tissue opacity in the right cervical region (Fig 1). No other abnormalities were observed on the radiographs. Because of the size of the mass and the bird's weight loss, surgical treatment was elected. The skin overlying the mass was plucked of feathers, aseptically prepared, and draped in a standard sterile manner. Bipolar electrosurgery (Ellman International, Hewlett, NY, USA) was used to incise the skin overlying the mass. Grossly, the mass appeared to be well vascularized and closely adhered to the esophagus, but no invasion into the esophagus was observed (Fig 2). Blunt and sharp dissection along fascial planes were used to free the mass from the esophagus. The right jugular vein was closely adhered to the cervical mass. During dissection, the right jugular vein was lacerated. Hemorrhage was controlled by using 2 small hemoclips (Weck Closure Systems, Research

Triangle Park, NC, USA). Intraoperative bradycardia and arrhythmias were controlled with atropine (0.7 mg/kg IM) and by reducing isoflurane concentration. The mass was removed and submitted for histopathologic examination. After copious lavage, the skin was closed with 5-0 polyglactin 910 (Vicryl; Ethicon Inc, Somerville, NJ, USA) in a Ford interlocking pattern. Recovery from anesthesia was rapid and uneventful. After surgery, the bird was treated supportively with ceftiofur sodium (13 mg/kg SC q24h x 6 days; Naxcel, Pfizer, New York, NY, USA), famotidine (1.3 mg/kg SC q24h x 3 days), meloxicam (0.2 mg/kg SC q24h x 3 days; Metacam, Boehringer Ingelheim Vetmedica Inc, St Joseph, MO, USA), and Normosol-R (10 mL SC the day of surgery, then 5 mL SC q24h x 2 days) to control pain and any possible esophagitis secondary to manipulation during surgery.

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During the first 3 days after surgery, the bird was lethargic, weak, and anorectic. When approached, the bird would become active and attempt to bite. On the fourth day after surgery, dried fluid was present in the region of the incision with focal areas of skin necrosis surrounding the suture line. The oral cavity was malodorous and local areas of necrosis were present. A mixed bacterial population was identified on cytologic evaluation of the oral cavity, with a predominance of gram-positive cocci. Trichomonas organisms were not visualized. The owl was force fed a pinkie mouse.

On the fifth day, the owl was alert, wide-eyed, and perching on the water bowl, and it had consumed 2 pieces of prey items. No further discharge was observed from the incision site, but the oral cavity was still malodorous with mucoid discharge. Normosol (7 mL SC q24h x 2 days), sucralfate (46 mg/kg PO q12h x 2 days), and meloxicam (0.2 mg/kg SC q24h x 2 days) were initiated to treat presumptive esophagitis.

On day 6, large areas of necrotic skin were present at the incision site and the foul odor from the oral cavity was stronger. The owl did not resist manual restraint and was very lethargic. Nutritional support was provided by gavage of 4 mL dilute (1:1) semisolid canned food (a/d, Hill's Pet Nutrition, Topeka, KS, USA), which was regurgitated. Gavage feeding, wound debridement, and esophagoscopy were planned for the next day but the bird died overnight.

Necropsy examination revealed a thin bird with a foul-smelling oral cavity. Dried serous discharge surrounded the incision. A large necrotic ulcer was present in the esophagus with food and caseous material in the subcutaneous space. No gross perforations of the esophagus were present. The intestines appeared necrotic.

The resected mass was greatly expansile, but there was no evidence of local invasion or distant metastasis. Microscopically, the mass consisted of densely cellular nests and sheets separated by connective tissue. The cells had indistinct cell margins and abundant, finely granular, pale eosinophilic cytoplasm with polygonal nuclei that contained reticular chromatin and prominent, often multiple nucleoli, and marked anisokaryosis. Mitoses were rare, one per 7 high power (40x) fields. There were numerous mature lymphocytes and lesser numbers of plasma cells admixed with the neoplastic cells. On the periphery of the mass there were several cystic structures that were lined by low cuboidal or attenuated epithelium. Many of these contained granular eosinophilic material, red blood cells, and occasional nests and clusters of neoplastic cells and lymphocytes. The tumor was an epithelial variant of a thymoma (Figs 3 and 4).

In addition to the thymoma, histologic examination of tissues collected at necropsy revealed a section of the esophagus that had extensive transmural necrosis and inflammation with numerous colonies of fine bacilli present. Moderate intratubular urate stasis and mild renal tubular mineralization were most likely related to dehydration. A marked, subacute, periportal hepatitis was observed and was considered to be secondary to the bacterial esophagitis.

Discussion

In all avian species, the differential diagnosis for a cervical swelling is fairly extensive and includes foreign body reaction, trauma, fungal granuloma, abscess, and neoplasia? Additionally, in strigiform species, esophageal pellets are regurgitated one to two times per day and must also be on the differential diagnosis list when a cervical swelling is encountered. (2) In this owl, cervical swelling was observed 6 months earlier during a period of lethargy. Radiographs performed at that time demonstrated mineral opacities in the lateral cervical region, consistent with bones from prey items. However, it is possible that the mass was present at that time but not diagnosed.

The avian thymus consists of 3-8 lobes of tissue that traverse lateral to the trachea, following the course of the jugular vein in the cervical region. (3,4) The biological behavior of thymomas are benign and the neoplasia arises from the epithelial portion of the thymus. (5)

Thymomas are rarely reported in avian species and have only been documented in an African grey parrot (Psittacus erithacus), (1) a finch (unspecified species), (6) domestic chickens, (7,8) a budgerigar (Melopsittacus undulatus), (9) and a Java sparrow (Padda oryzivora). (10) Birds with thymomas commonly present with dyspnea, malaise, dysphagia, or a palpable mass in the cervical region, (1) some of which were present in this case.

Multiple retrospective studies have investigated diagnosis, treatment, and long-term survival in dogs and cats with thymomas. (11-15) Common diagnostic modalities used to identify thymomas are [sigma] radiography, ultrasonography, fine-needle aspiration (with or without ultrasound guidance), computed tomography (with or without contrast enhancement), and needle biopsy. (14,16-18) Surgical excision is curative in most noninvasive thymomas and is commonly performed. (11-14,19) Radiotherapy and chemotherapy may be useful in dogs and cats with nonresectable thymomas, although when used alone, these treatment modalities rarely result in complete and long-lasting remission (5,13,15,20,21) Integration of radiotherapy, chemotherapy, and surgery can contribute to improved long-term outcome in advanced thymomas. (5,12,13,15,20,21) Although the thymus is located in the cervical region in avian species, similar diagnostic and therapeutic techniques should be considered.

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In all previously reported avian thymomas, limited presurgical diagnostics were performed before attempted mass resection. Ideally, a complete diagnostic work-up consisting of complete blood count, plasma biochemical analysis, radiographs, and computed tomography would be performed before surgical exploration. Fine-needle aspirate with cytologic evaluation or biopsy are useful diagnostic modalities that can be used for an accurate preoperative diagnosis. In small animals, computed tomography is particularly useful in determining if the mass is invading the cranial vena cava, and this imaging modality holds promise in helping evaluate cervical masses in avian species. In this case, computed tomography would have provided valuable information regarding the tumor's adherence to the jugular vein and esophagus, allowing the surgeon to better plan the approach.

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Treatment of thymomas in avian species has largely been unrewarding except for one report of a surgical excision in a Java sparrow with a small mass (1.5 x 2.0 cm) that was not infiltrating surrounding tissue. (10) No discussion of alternate treatment modalities such as radiotherapy or chemotherapy have been reported, although these modalities have been used successfully in canine and feline clinical cases and would be useful treatment modalities to explore in cases of thymomas invading the jugular vein. Currently, surgical resection is the only described treatment option for noninvasive thymomas in avian species. In birds, if there is thymoma invasion into the jugular vein, chemotherapy or radiotherapy should be considered.

The size of the thymoma, proximity to the right jugular vein, and adherence to the esophagus likely contributed to the postoperative complications experienced in this case. In companion animals, it has been documented that cases of thymoma invasion into large vessels (ie, vena cava) have a less favorable postoperative prognosis when compared with noninvasive thymomas. (14,17) Avian thymomas are likely similar to companion animal thymomas in this respect, with vascular invasion carrying a worse prognosis. Compression of the esophagus from the thymoma and surgical dissection likely caused traumatic injury and vascular compromise to the cervical esophagus, contributing to the necrosis, postoperative feeding difficulties, and ultimately the bacterial esophagitis.

This case illustrates 2 important points regarding surgical thymoma resection in avian patients. First, the surgeon must be prepared to encounter thymoma adhesion to or invasion of the jugular vein during excision of the mass and should be equipped to achieve hemostasis quickly even though the prevalence of vascular involvement of thymomas in avian patients is unknown. Secondly, postoperative feeding difficulties should be anticipated and a plan should be developed to provide nutritional support in an anorectic bird that may include gavage feeding or an esophagostomy tube. Although the outcome may not have changed in this case, the patient would have likely benefited from being force-fed within the first 24 hours when it was not eating on its own.

Thymoma must be considered as a differential diagnosis when an avian patient presents with a cervical mass. In strigiform species, esophageal pellets also must be ruled out. This can be done by taking a thorough patient history, including time of last feeding. Demonstrating mineral opacities within the mass provides radiographic evidence of a pellet. When still uncertain, contrast radiography can be used to differentiate cervical masses from esophageal pellets. Additional diagnostic tests such as ultrasonography, computed tomography, fine-needle aspiration, and biopsy can help identify the origin of the mass and assist in determining possible treatment options. When surgical excision of a thymoma is elected, evaluating the extent of esophageal adhesion or invasion is important. Care must be taken to determine involvement of the jugular vein, particularly if the mass is in the right cervical region. Potential complications associated with postoperative feeding must be carefully considered when resecting thymomas in birds.

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Matthew E. Kinney, DVM, Christopher S. Hanley, DVM, Dipl ACZM, and John G. Trupkiewicz, DVM, Dipl ACVP

From the University of Wisconsin, School of Veterinary Medicine, 2015 Linden Dr, Madison, WI 53706, USA (Kinney); The Toledo Zoo, 2700 Broadway St, Toledo, OH 43607, USA (Hanley); and the Northwest Zoopath, 654 W Main St, Monroe, WA 98272, USA (Trupkiewicz). Present address: University of California, School of Veterinary Medicine, One Shields Ave, Davis, CA 95616, USA (Kinney); Philadelphia Zoo, 3400 W Girard Ave, Philadelphia, PA 19104, USA (Trupkiewicz).
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