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External beam radiation therapy of squamous cell carcinoma in the beak of an African grey parrot (Psittacus timneh).

Abstract: Squamous cell carcinoma has been reported in a variety of bird species, most commonly psittacine and gallinaceous birds. The long-term prognosis in nongallinaceous birds is generally poor if complete surgical excision is not possible. Squamous cell carcinoma of the rhinotheca was diagnosed in a 34-year-old timneh African grey parrot (Psittacus timneh) with a 2year history of beak abnormalities. No evidence of metastasis or local invasion were found on results of radiographs or computed tomography scan. The bird was treated with surgical debulking and palliative megavoltage radiation therapy. After 4 radiation treatments, the affected tissue was necrotic and was debrided to reveal healthy granulation tissue. The bird died approximately 7 months after diagnosis and 4 months after cessation of radiation treatment. At the time of death, a small scab lesion remained at the left oral commissure, but no visible tumor regrowth was evident. A postmortem examination was not performed, however, and tumor recurrence could not be ruled out in this bird.

Key words: squamous cell carcinoma, neoplasia, radiation therapy, beak, psittacine, avian, African grey parrot, Psittacus timneh

Clinical Report

A 34-year-old male timneh African grey parrot (Psittacus timneh) was referred to the Exotic Animal Medicine Service at the North Carolina State University Veterinary Hospital (NCSU VH) for evaluation of a severely diseased maxillary beak. The beak abnormalities had been observed for at least 2 years and included a progressive thickening of the left side of the rhinotheca and elongation of both the rhinotheca and gnathotheca. The overgrown keratin had been managed with frequent corrective trimming. Eleven months before presentation, a fungal culture of the proliferative material trimmed from the left rhinotheca grew Alternaria and Penicillium species. The bird had been treated with repeated 2M-week courses of enrofloxacin (14 mg/kg PO q24h) and itraconazole (7 mg/kg PO q24h) systemically. The affected area of the beak was being cleaned with chlorhexidine solution and treated with a topical application of thiabendazole/dexamethasone/neomycin solution (Tresaderm, Merial, Duluth, GA, USA) daily. The owner reported that these treatments initially decreased the frequency with which trims were required, but the beak abnormalities recurred and worsened over the 6 months before presentation. The bird was housed in a cage in an indoor aviary with a red-crowned Amazon parrot (Amazona viridigenalis) and fed a diet consisting primarily of pellets (Daily Maintenance, Roudybush Inc, Woodland, CA, USA), with occasional treat balls (Nutri-Berries, Lafeber Company, Cornell, IL, USA), vegetables, peanuts, and table food as treats. There was no known history of trauma, except for an aggressive beak trim performed 3-4 years earlier, which reportedly resulted in a full-thickness keratin defect on the left side of the rhinotheca.

On initial physical examination, the bird was in good body condition (body condition score 3.5/5) and weighed 292 g. Both the rhinotheca and the gnathotheca were markedly overgrown, and the distal third of the rhinotheca was deviated to the right. The left side of the rhinotheca was obliterated by irregular, friable tissue from the naris to the tip and extending from the culmen to the palate (Fig 1). When the beak was manipulated, a small amount of bleeding was noted from the caudal aspect of the tomium at the commissure of the mouth. No other abnormalities were noted on physical examination. The results of a complete blood count (CBC) revealed a normal white blood cell count (10.04 X [10.sup.3] cells/[micro]L; reference interval, 5-15 X [10.sup.3] cells/[micro]L), with a relative heterophilia (94%; reference interval, 45%-75%), lymphopenia (2%; reference interval, 20%-50%), and monocytosis (4%; reference interval, 0%-3%). (1) Results of the biochemical panel were within reference intervals for the species, with the exception of an increase concentration of aspartate aminotransferase (445 U/L, reference interval 100-350 U/L). (1) The elongated gnathotheca was trimmed and shaped with a conical aluminum oxide attachment on a Dremel multitool (Robert Bosch Tool Corporation, Racine, WI, USA). The rhinotheca was not trimmed because of concerns about hemorrhage and discomfort in the unanesthetized bird. Topical steroid treatment was discontinued, and the systemic antifungal agent was changed from itraconazole to fluconazole (15 mg/kg PO q12h) because of the anecdotal sensitivity of African grey parrots to itraconazole. (1) Differential diagnoses considered at this time for the keratin overgrowth included previous trauma to the germinal tissue of the beak, bacterial or fungal infection of the beak, neoplasia, or liver disease. (2) Diagnostic imaging was recommended to further assess the extent of the lesion before surgical biopsy and to evaluate for evidence of systemic disease.

Radiographs and a whole-body computed tomography (CT) scan were performed the next week. The patient was premedicated with calcium gluconate (10 mg/kg IM) diluted 1:1 with sterile water and induced and maintained on isoflurane (2%-3%). A brief episode of second degree atrioventricular block occurred that resolved without treatment while under anesthesia. Whole-body radiographs revealed no significant abnormalities, other than the abnormal beak. Results of the CT scan (Fig 2) revealed mild periosteal reaction of the premaxillary bone on the left side, but no evidence of cortical lysis or local extension of disease into the sinuses or nasal cavity. No evidence of distant metastasis was detected on radiographs or CT scan. Surgical biopsy of the affected area of the beak was recommended.

Two weeks later, the bird returned for surgical debridement of the lesion. It was premedicated with butorphanol (1 mg/kg IM; Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) and calcium gluconate (10 mg/kg IM). Because of the previously noted arrhythmia, the anesthetic agent was changed from isoflurane to sevoflurane (5%6%). (3) The grossly abnormal tissue overlying the left maxillary beak was removed en bloc by blunt dissection, exposing underlying dermis from the left naris to the distal aspect of the beak. Excessive keratin was trimmed from the right side of the maxillary beak. The tissue bed on the left side of the maxillary beak was friable and vascular. Hemorrhage was controlled with silver nitrite applicators, absorbable gelatin sponge (Gelfoam, Pfizer Inc, New York, NY, USA), and application of a pressure bandage. The excised tissue was submitted for histopathologic examination and bacterial and fungal culture. Within hours of the surgery, the bird was eating soft and liquid foods, and the bandage was removed the next day with no significant ongoing hemorrhage observed. The beak was treated with low-level laser therapy (0.4 W X 48 seconds, total 19 J over 2 [cm.sup.2]; K-Laser Cube, Franklin, TN, USA) for 2 days after surgery to promote healing. The surgical site was cleaned twice daily with povidone iodine scrub and covered in a thin layer of 1% silver sulfadiazine cream. The bird also was started on meloxicam (0.5 mg/kg PO q24h) and enrofloxacin (15 mg/kg PO q12h) and was continued on fluconazole, pending culture results.

On histopathologic examination, approximately 80% of the excised tissue consisted of orthokeratotic hyperkeratosis. However, the deep margin was lined with unencapsulated, poorly demarcated, highly cellular tissue, exhibiting anisocytosis and anisokaryosis and 15 mitotic figures per 10 high-power fields (Fig 3). The histologic appearance of the lesion was most consistent with squamous cell carcinoma. Aerobic bacterial culture revealed heavy growth of penicillin-resistant Staphylococcus pseudintermedius and scant growth of multi-drug-resistant Stenotrophomonas maltophilia. Biphasic fungal culture revealed light growth of Candida species. Based on the culture and sensitivity results, the antibiotic was changed to trimethoprim/sulfamethoxazole (30 mg/kg PO q12h), and systemic antifungal treatment was discontinued. Meloxicam and topical wound treatments were continued.

On recheck examination 12 days after surgery, the surgical site on the left maxillary beak was covered with black, firm, irregular tissue. Ventral to the left naris and extending to the commissure of the mouth, the tissue was pink to yellow and slightly raised. Although regrowth of the tumor in this tissue was suspected, a second biopsy was not done to confirm this suspicion. The skin from the left eye to the naris was light purple, which was likely the result of bruising (Fig 4). The bird's weight was unchanged and the owner reported that it was eating soft foods well at home.

After discussion of treatment options, the owner elected to pursue palliative-intent external beam radiation therapy (RT). The first treatment was administered 6 weeks after surgical debridement. At this time, the results of a CBC revealed normal white blood cell count with a relative heterophilia (84%), lymphopenia (9%), and monocytosis (7%), similar to previous results. (1) The plasma biochemical results were unremarkable. A manual (nongraphic) radiation treatment plan was created with the bird under anesthesia immediately before the first dose of RT. A linear accelerator (Novalis linear accelerator, Yarian Medical Systems, Palo Alto, CA, USA) was used to deliver 8 Gy once weekly for 4 weeks, resulting in a total dose of 32 Gy. The radiation was prescribed to midline via a source-to-axis calculation and delivered to the entire maxillary beak with 6 MV photons via parallel opposing fields. Bolus material was placed in the oral cavity to improve dose homogeneity and increase the radiation dose administered to the superficial aspect of the tumor. The eyes were covered to minimize radiation dose to that tissue. For each treatment, the patient was premedicated with butorphanol (1 mg/kg IM) and calcium gluconate (10 mg/kg IM) and induced and maintained on sevoflurane (5%-6%) with a pressure-driven ventilator (Vetronic Small Animal Ventilator, Newton Abbot, Devon TQ12, UK).

Over the course of the first 2 weeks of radiation treatment, firm black tissue continued to proliferate from the caudal aspect of the left maxillary beak, extend rostrally and medially across the palate, and expand laterally. The beak began to appear much as it did before surgery, but the new tissue was not friable. On week 3 of radiation treatment, an area of malodorous, caseous material was noted on the palate near the choana, and the bird was again started on trimethoprim/ sulfamethoxazole (30 mg/kg PO q12h for 2 weeks). The owners reported that the bird continued to eat well at home, and they did not note any change in behavior.

On week 4 of radiation therapy, a malodorous, purulent exudate was observed under the abnormal tissue on the left maxillary beak and the skin from the left eye to the left naris was discolored dark purple. With the bird under general anesthesia, the layer of thick, firm, dark tissue covering the caudal half of the left maxillary beak was sharply debrided to reveal friable, necrotic soft tissue and caseous debris (Fig 5).

Over the next 2 weeks, most of the remaining necrotic tissue overlying the left beak sloughed off. On re-evaluation at NCSU VH during this time, the beak was cleaned and a small amount of residual necrotic tissue was debrided from the left lateral beak after applying topical lidocaine (0.03 mL of a 20 mg/mL preparation diluted 1:10 with sterile water) to the surrounding tissue. Loss of the necrotic tissue resulted in exposure of the dermis overlying the maxillary bone from the caudal aspect of the left side of the maxillary beak to the tip of the beak, including the entire rostral third of the beak. The only part of the maxillary beak that remained covered by normal keratin was the caudal two-thirds of the right side extending from the oilmen to the tomium.

Forty days after the final radiation treatment, the patient was presented for a recheck examination and a corrective mandibular beak trim. There was evidence of some re-epithelialization of the left side of the beak, but most of the tissue was covered with a thin layer of yellow debris. A thicker layer of debris overlying the area from the left naris to the commissure was removed with gentle cleaning to reveal a slightly raised bed of pink tissue underneath. Although it appeared that healthy granulation tissue was present in this region, the possibility of tumor regrowth was also considered. Results of a CBC revealed a mild anemia (37%) and leukopenia (2.7 x [10.sup.3] cells/[micro]L). Results of a biochemical panel revealed hypophosphatemia (2 mg/dL; reference interval, 3.2-5.4 mg/dL) and mild hypoalbuminemia (1.4 g/dL; reference interval, 1.57-3.23). (1)

When the parrot was presented 1 month later for another mandibular beak trim, the maxillary beak remained shortened and misshapen, but it was almost entirely covered in a thin layer of nonkeratinized epithelium. Most of the palate was lined with a pale pink epithelium and a small scabbed area remained at the left commissure. This persistent lesion was approximately half the size that it had been 1 month before (Fig 6). The bird was in heavy molt and had lost 25 g since the previous visit. However, the owners felt that they had been less proactive about providing the bird with soft food, so the clinical significance of the weight loss was unclear. The bird died at home soon after this last recheck and was not returned for a full postmortem examination.

Discussion

The results of the treatment of the bird in this report suggest that palliative external beam radiation therapy holds promise as a therapeutic modality for squamous cell carcinoma of the beak in birds. In this case, suspected rapid tumor regrowth was arrested and tumor burden was markedly decreased after palliative external beam radiation. However, recurrence of the tumor after radiation could not be ruled out at the time of death of this bird.

Squamous cell carcinoma has been reported in a variety of avian species, including psittacine birds,4-10 gallinaceous birds, (11,12) raptors, (13,14) a hornbill (Buceros biconus). (15) a common stork (Ciconia ciconia), (16) a pelican (Pelecanus rufescens), (17) and a flamingo (Phoenicopterm ruber). (18) In chickens, dermal squamous cell carcinoma has been associated with poxvirus, but these lesions tend to behave very differently from squamous cell carcinoma in other species; they are generally multicentric and often spontaneously regress." No relationship has been reported between poxvirus and squamous cell neoplasia in psittacine birds.

Various treatment modalities have been attempted for squamous cell carcinoma in birds, including surgical excision, (4,6,14,16) photodynamic therapy, (10,15) intralesional cisplatin. (5) external beam radiation, and combinations thereof. (8,13,18) Most reported survival times range from weeks to months, with only a few reports of long-term control or clinical cure. A recent survey-based study of squamous cell carcinoma in birds reported a median survival time of 341 days after diagnosis and found that surgical excision (when possible) was the only treatment associated with significantly increased odds of a partial or complete response to therapy. (19) Metastasis in birds appears to be relatively uncommon, with only 2 cases reported (9,14); sites of metastasis include lungs, bone, and spleen.

Limited information is available about the use of external beam radiation therapy for treatment of neoplasia in birds, especially around the beak and oral cavity. (20) Tumors treated with radiation therapy have included squamous cell carcinoma, (8,13,18) hemangiosarcoma, (21) fibrosarcoma, (22,23) malignant melanoma, (24) and osteosarcoma. (23) Reported protocols have included the use of orthovoltage radiation, (23,25) strontium-90, (13) cesium-137, (21) cobalt-60, (8,18,22) and linear acceleration (24) with mixed success. Total number of treatments ranged from 1 to 20, and total dose ranged from 40 to 150 Gy.

Birds are thought to have a higher radiation tolerance than mammals, although the data to support this supposition is limited. The one published study of radiation dose tolerance in birds administered megavoltage radiation in 4-Gy fractions to the ingluvial area of ring-necked parakeets (Psittacula krameri) up to a total dose of 72 Gy without ill effects. (26) Reported acute radiation effects in birds include feather loss, erythema, edema, and skin necrosis. (22-24) Most cases in which local side effects were reported were also treated with intralesional cisplatin. To our knowledge, no chronic radiation side effects have been reported in birds.

Management of neoplasia of the beak is challenging because in most cases it is impossible to obtain sufficient margins with surgical management. While successful beak amputation has been reported in psittacine birds, (27) the procedure carries significant risks and can potentially have a long-term effect on the bird's quality of life. In this particular case, beak amputation was not considered a viable alternative because the amputation would not have produced adequate margins at the caudal aspect of the mass. In cats, radiation is often used as a sole or adjunctive therapy for oral squamous cell carcinoma in locations where it is impossible to achieve adequate surgical margins. (28,29) The largest retrospective study of outcomes in cats with oral squamous cell carcinoma treated with palliative-intent radiation therapy found that mean survival time was 127 days. Subjective improvement in quality of life was reported by 59% of owners, and most patients had mild or no side effects. (29) Unfortunately, because the behavior of squamous cell carcinoma is highly variable by site, species, and individual, extrapolating these data to predict outcome in an individual avian patient is difficult.

Only one other report described the use of external beam radiation therapy to treat squamous cell carcinoma of the beak in a Buffon's macaw (Ara ambiguus). (8) The bird received 12 cobalt-60 treatments of 4 Gy (3 treatments weekly for 4 weeks) and a single booster dose of 8 Gy 15 weeks later. The tumor showed no gross or histologic evidence of response to the radiation. Survival from time of diagnosis was 31 weeks, and the bird displayed anorexia and significant weight loss over the course of treatment; however, management was complicated by severe abscessation and osteomyelitis of the beak. Although a recent study found that only surgical intervention was associated with improved outcome, this study did not specifically evaluate megavoltage radiation therapy as a treatment modality. (19)

In our case, the behavior of the tumor is difficult to comment on with certainty, because histologic confirmation of neoplasia was only available at one time point in the progression of the disease. The patient's history suggests that the tumor may have been present and relatively slow growing for at least 2 years before presentation, but evidence of potential rapid tumor regrowth was present soon after surgical debridement. Tumor growth may have been slow initially and accelerated after surgical debridement as a result of decreased pressure or increased oxygenation. Because biopsy samples were not taken at the onset of visible rhinothecal abnormalities, the initial changes observed for the 2 years before referral possibly represented a chronic inflammatory process that underwent malignant transformation later in the disease progression. It is also possible that the rapid tissue regrowth after surgery represented a benign proliferative response to damage sustained by the germinal tissue of the rhinotheca and not regrowth of tumor. Whether the necrosis of the palate after the start of RT was secondary to mucositis as a side effect of the radiation or whether it represented local invasion by the tumor is unclear.

Unfortunately, a postmortem examination was not performed, so the cause of death in this bird is unknown. Metastatic neoplasia cannot be ruled out but is thought to be relatively uncommon with squamous cell carcinoma in birds.

No acute radiation adverse effects were noted, although the bird did not survive long enough to rule out the possibility of late radiation effects. No apparent evidence of chronic radiation adverse effects was noted at the patient's last examination. After maintaining a consistent body weight throughout treatment, it had experienced significant weight loss (25% of body weight) over approximately 5 weeks. Whether this weight loss was associated with undetected systemic disease or a result of difficulty eating due to beak pain or malocclusion is unclear.

Because the response of squamous cell carcinoma is highly variable by location and by individual, a large sample size will be necessary to determine the true value of radiation as a therapeutic modality for treatment of squamous cell carcinoma in psittacine birds. Further study is needed to determine optimal protocols for irradiation of the beak and to evaluate the responsiveness of various types of avian neoplasia to radiation.

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Samantha D. Swisher, DVM, Kathryn L. Phillips, DVM, Dipl ACVR, Jeremy R. Tobias, DVM, Dipl ACVP, John M. Cullen, VMD, PhD, Dipl ACVP, Tracy L. Gieger, DVM, Dipl ACVIM, Dipl ACVR, and Vanessa L. Grunkemeyer, DVM, Dipl ABVP (Avian)

From the Department of Clinical Sciences (Swisher, Gieger, Grunkemeyer), the Department of Molecular Biomedical Sciences (Phillips), and the Department of Population Health and Pathobiology (Tobias, Cullen), College of Veterinary Medicine, North Carolina State University, 1060 William Moore Dr, Raleigh, NC 27607, USA. Present addresses: Avian & Exotic Animal Clinic of Indianapolis, 9330 Waldemar Rd, Indianapolis, IN 46268, USA (Swisher): Department of Surgical and Radiological Sciences, College of Veterinary Medicine, University of California Davis, 2112 Tupper Hall, One Shields Ave, Davis, CA 95616, USA (Phillips); Department of Biological Sciences, College of Life Sciences and Agriculture, University of New Hampshire, 214 Kendall Hall, 129 Main St, Durham, NH 03824, USA (Grunkemeyer).
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Author:Swisher, Samantha D.; Phillips, Kathryn L.; Tobias, Jeremy R.; Cullen, John M.; Gieger, Tracy L.; Gr
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Sep 1, 2016
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