UROPYGIAL GLAND SQUAMOUS CELL CARCINOMA IN CHINSTRAP (PYGOSCELIS ANTARCTICUS) AND GENTOO (PYGOSCELIS PAPUA) PENGUINS AT THE WILDLIFE CONSERVATION SOCIETY'S CENTRAL PARK ZOO Author(s): Christy L. Rettenmund, D.V.M., Alisa L. Newton, V.M.D., Dipl. A.C.V.P., and Paul P. Calle, V.M.D., Dipl. A.C.Z.M. Source: Journal of Zoo and Wildlife Medicine, 46(1):113-119. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2014-0011R1.1 URL: http://www.bioone.org/doi/full/10.1638/2014-0011R1.1

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Journal of Zoo and Wildlife Medicine 46(1): 113–119, 2015 Copyright 2015 by American Association of Zoo Veterinarians

UROPYGIAL GLAND SQUAMOUS CELL CARCINOMA IN CHINSTRAP (PYGOSCELIS ANTARCTICUS) AND GENTOO (PYGOSCELIS PAPUA) PENGUINS AT THE WILDLIFE CONSERVATION SOCIETY’S CENTRAL PARK ZOO Christy L. Rettenmund, D.V.M., Alisa L. Newton, V.M.D., Dipl. A.C.V.P., and Paul P. Calle, V.M.D., Dipl. A.C.Z.M.

Abstract: Uropygial, or preen, glands are found in a variety of avian species including penguins. These glands have a multitude of functions and can develop a variety of conditions including impaction, rupture, adenitis, squamous metaplasia, and neoplasia of various types, with squamous cell carcinoma the most commonly reported. A case series of uropygial gland squamous cell carcinoma in five penguins at the Wildlife Conservation Society’s Central Park Zoo is described. Most birds were aged (.10 yr) with a history of chronic, recurrent uropygial gland problems including impaction, rupture, abscess formation, or a combination of conditions. Before and after neoplasia diagnosis, these cases were managed conservatively, and palliative care was provided. Because many of these cases were preceded by chronic inflammation, it is possible this inflammation predisposed the uropygial gland to neoplastic transformation, and more aggressive treatment early in the disease process may therefore be warranted. Key words: Neoplasia, penguin, Pygoscelis antarcticus, Pygoscelis papua, squamous cell carcinoma, uropygial gland.

BRIEF COMMUNICATION Most avian species, including penguins, have a uropygial gland. The uropygial gland, also known as the preen or oil gland, is a bilobed holocrine gland located at the dorsal base of the tail above the levator muscles of the pygostyle. The gland secretions pass through ducts to openings at a caudally directed papilla that is generally surrounded by a tuft of feathers.3 This gland produces a complex mixture of monoester waxes, formed of fatty acids and monohydroxy wax alcohols that are distributed over the feathers by preening.13,22 The gland secretions are thought to have a variety of functions, including assistance in feather condition and waterproofing, protection against microorganisms such as feather-degrading bacteria and mycotic organisms, and inclusion of vitamin D3 precursors, which are photoconverted to cholecalciferol and ingested during preening.3,9,10,26,35,40,41 The secretions also serve odorant or pheromonal functions, or both, in some species including petrels, musk ducks (Biziura lobata), and kakapos (Strigops habroptilus).38

From the Wildlife Conservation Society, Zoological Health Program, 2300 Southern Boulevard, Bronx, New York 10460, USA (Rettenmund, Newton, Calle). Correspondence should be directed to Christy Rettenmund ([email protected]).

Abnormalities of the uropygial gland that have been reported in various avian species include impaction, rupture, adenitis, squamous metaplasia, and neoplasia. Squamous cell carcinoma is the most commonly reported neoplasia, although adenocarcinoma and adenoma also occur.3,30 In penguins, uropygial gland rupture and two cases of neoplasia have been reported: one malignant melanoma and one squamous cell carcinoma.18,21,37 This paper describes the clinical signs, treatment, and diagnostic findings for a series of uropygial gland squamous cell carcinomas in chinstrap (Pygoscelis antarcticus) and gentoo penguins (Pygoscelis papua) at the Wildlife Conservation Society’s Central Park Zoo (New York City). This is the third report of uropygial gland neoplasia in penguins but the first report of neoplasia involving either gentoo or chinstrap penguins. The Central Park Zoo houses an average of 66 penguins in a large climate-controlled exhibit with a 48,000 gallon freshwater pool and 1,300 square feet of gunnite rockwork and beach area for haul out. The colony currently consists of gentoo, chinstrap, king (Aptenodytes patagonicus), and rockhopper (Eudyptes chrysocome) penguins. Gentoo (n ¼ 24) and chinstrap (n ¼ 31) make up the majority of the penguins in the colony. They are fed a diet of capelin (Mallotus villosus), herring (Clupea harengus), silversides (Menidia menidia),

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22 mo Biopsy Not applicable Postmortem examination Clinical signs occurred intermittently during this time period. a

10 mo Biopsy Not applicable Postmortem examination

1 wk Biopsy

10 yra 4 yra 1 wk 8 yra 2 yr

Duration of clinical signs before definitive diagnosis Duration of treatment after definitive diagnosis Diagnosis confirmed

Gentoo 10 Enlarged gland Impaction, rupture, bleeding Chinstrap 10 Enlarged gland Impaction, abscess, ulceration Chinstrap 22 Bleeding gland Rupture, bleeding Chinstrap 5 Enlarged gland Impaction, fistula Gentoo 13 Enlarged gland Impaction, abscess, ulceration Penguin species Age of onset of clinical signs (yr) Presenting complaint Uropygial gland examination findings

4 3 2 1

and krill (Euphausia superba) supplemented with a half-tab multivitamin per penguin (Mazurit VitaZu bird tablets, St. Louis, Missouri 63166, USA) once daily. Wildlife Conservation Society penguin postmortem examination and biopsy records from 2000 to 2013 were reviewed. Five penguins with a confirmed diagnosis of uropygial gland squamous cell carcinoma were identified and are included in this case series. Three were diagnosed via biopsy and two at postmortem examination. All animals were initially examined for an abnormality of the uropygial gland. Clinical findings are summarized in Table 1. Case 3 differs from the others in that this animal had an acute onset of bleeding and rupture of the uropygial gland rather than the chronic, progressive disease observed in other penguins. Many treatment modalities were administered in four individuals for their uropygial gland disease before neoplasia diagnosis, with diseasefree intervals in animals with chronic uropygial gland disease (Table 2). Case 1 was treated with dilute Nolvasant flushing (Pfizer Animal Health, New York, New York 10017, USA) and infusion with nystatin-neomycin sulfate–thiostrepton–triamcinolone acetonide ointment (Animaxt, Foster and Smith Inc., Rhinelander, Wisconsin 54501, USA) one to two times weekly, which resulted in resolution of the uropygial gland impaction after 5 wk. However, 10 mo later, an abscess of the gland developed. It was unresponsive to 3 wk of topical (dilute Nolvasan solution, Animax infusion) and systemic antimicrobial therapy (enrofloxacin 19 mg/kg p.o., s.i.d., Bayer Animal Health, Shawnee Mission, Kansas 66216, USA; metronidazole 23 mg/kg p.o., s.i.d., Teva Pharmaceuticals, North Wales, Pennsylvania 19454, USA; itraconazole 9 mg/kg p.o., s.i.d., Centocur Ortho Biotech Products, L.P. Ravitan, New Jersey 08869, USA), but resolution was observed after surgical debridement and topical Animax for an additional 2 wk. Three months later, the abscess reoccurred and was unresponsive to treatment with Animax, silver sulfadiazine (Watson Laboratories Inc., Corona, California 92880, USA), trimethoprim sulfamethoxazole (22 mg/kg p.o., s.i.d., Amneal Pharmaceuticals, Hauppauge, New York 11788, USA), surgical debridement, and bandaging over the course of 6 mo. Surgical removal of the gland was elected, but the animal died under anesthesia. In contrast to case 1, cases 2 and 4 were similar in that both initially had multiple instances of uropygial gland impactions (n ¼ 6) over 7–8 yr, which responded within 2–8 wk to topical dilute

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Table 1. Summary of the five cases of uropygial gland squamous cell carcinoma in chinstrap (Pygoscelis antarcticus) and gentoo penguins (Pygoscelis papua) at the Wildlife Conservation Society’s Central Park Zoo.

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a

SSD, silver sulfadiazine; TAO, triple antibiotic ointment; TMS, trimethoprim sulfamethoxazole; CCFA, ceftiofur crystalline free acid.

Yes Meloxicam, CCFA, butorphanol, dilute Nolvasan, Animax No Not applicable Yes Enrofloxacin, itraconazole, butorphanol Yes Butorphanol Yes Not applicable Surgical debridement? Treatments postdiagnosis

Gentoo Dilute Nolvasan, dilute Dawn, Animax, TAO, iodoform tape Enrofloxacin, itraconazole, doxycycline, butorphanol Chinstrap Dilute Nolvasan, Animax, TAO Enrofloxacin, itraconazole Chinstrap Dilute Nolvasan Enrofloxacin, itraconazole, butorphanol Chinstrap Dilute Nolvasan, Dilute Dawnt, Animax Enrofloxacin, metronidazole, itraconazole Gentoo Dilute Nolvasan, Animax, SSDa Enrofloxacin, metronidazole, itraconazole, TMS Penguin species Topical therapies prediagnosis Systemic therapies prediagnosis

5 4 3 2 1

Table 2. Summary of the treatment modalities instituted in chinstrap (Pygoscelis antarcticus) and gentoo penguins (Pygoscelis papua) before and after diagnosis with uropygial gland squamous cell carcinoma.

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Nolvasan or flushing with dilute dish detergent (Dawn, Proctor and Gamble, Cincinnati, Ohio 45201, USA) in combination with triple antibiotic ointment (Taro Pharmaceuticals USA Inc., Hawthorne, New York 10562, USA) or Animax infusion one to two times weekly. Systemic antimicrobial therapy (enrofloxacin [15–20 mg/ kg p.o., s.i.d.], metronidazole [27 mg/kg p.o., s.i.d.]) and itraconazole (10–14 mg/kg p.o., s.i.d.) were only administered when malodorous debris was present (case 2) or when abscess formation and ulceration occurred (case 4). Similar to cases 2 and 4, case 5 also had several occurrences (n ¼ 3) of uropygial gland impaction over 4 yr, which resolved in 2–8 wk postflushing with dilute Nolvasan or dilute Dawn in combination with Animax or triple antibiotic ointment. In this case, the impaction progressed to active bleeding, which was managed with surgical debridement, dilute Nolvasan flushing, iodoform umbilical tape packing, enrofloxacin (15 mg/kg p.o., s.i.d.), and itraconazole (22 mg/kg p.o., s.i.d.). Umbilical tape packing was not successful; however, resolution occurred after 3 wk of dilute Nolvasan flushing and triple antibiotic ointment infusions. One year later, marsupialization of the uropygial gland was performed because of the history of chronic impactions. Postoperative treatments included dilute Nolvasan flushing, triple antibiotic ointment infusion, enrofloxacin (15 mg/kg p.o., s.i.d.), butorphanol (1 mg/kg p.o., s.i.d., Akorn Inc., Decatur, Illinois 62522, USA) and itraconazole (22 mg/kg p.o., s.i.d.) administration until resolution 2 mo later. The impaction recurred two times over the next 2 yr but responded within 4–8 wk to dilute Nolvasan flushing and Animax infusion. One year later, malodorous debris was present on the gland. After 8 wk of treatment with doxycycline hyclate (45 mg/kg p.o., s.i.d., West-Ward Pharmaceutical Inc., Eatontown, New Jersey 07724, USA), dilute Nolvasan flushing, and Animax infusion, clinical signs resolved. Blood collection for complete blood count and chemistry panel was performed sporadically over the course of the disease process in three cases. In case 2, blood was collected for a complete blood count and chemistry panel during biopsy collection and all values were unremarkable.12 In case 4, blood was collected three times over the course of the disease. Blood work was initially unremarkable, but a few months before euthanasia (2 yr after initial blood sample), a leukocytosis (white blood cell count of 27,900 cells/lL, reference range 9,146 6 5,722 cells/lL) was present, which persisted until euthanasia.12 In case 5, blood was

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Figure 1. Postmortem examination image of a uropygial gland squamous cell carcinoma in a gentoo penguin (case 5).

collected four times over a 2-yr period. Initial blood work was unremarkable. However, 1 mo later, as the appearance of the uropygial gland worsened, a severe leukocytosis (white blood cell count of 35,900 cells/lL, reference range 12,420 6 4,371 cells/lL) was noted, whereas chemistry values remained unremarkable. Blood was collected 1 mo and 1 yr later when the animal was immobilized for surgical debridement and biopsy, and all values were within reference ranges.12 The diagnosis of squamous cell carcinoma was confirmed via uropygial gland punch biopsy in three birds before euthanasia (Table 2). In case 2, the penguin’s uropygial gland remained of normal appearance with no treatment for 7 mo after biopsy, after which the animal care staff noticed a new enlargement of the gland. Malodorous necrotic debris was debrided, although subsequent progressive necrosis of the gland occurred over the next 3 mo. Butorphanol tartrate (1.3 mg/kg p.o., s.i.d.) therapy was instituted, but the animal’s quality of life deteriorated, and euthanasia was elected 3 mo after gland enlargement was noted. Case 3 was treated with enrofloxacin (20 mg/kg p.o., s.i.d.), itraconazole (7.5 mg/kg p.o., s.i.d.), and butorphanol tartrate (0.8 mg/kg p.o., b.i.d.) post–biopsy collection but was euthanatized 2 wk later. Case 5 was managed for the longest duration (22 mo) postdiagnosis. This animal was initially treated with meloxicam (8 lg/kg s.c. once, Boehringer Ingelheim, 55218 Ingelheim am Rhein, Germany) and ceftiofur crystalline free acid (40 mg/kg i.m. once, Pfizer Animal Health) at the time of immobilization for biopsy. Four months after biopsy collection, the uropygial gland size increased and developed a fistula that extended

deep into the tissue. The gland was debrided and inspissated material removed every 3–4 mo as needed in combination with dilute Nolvasan flushing, instillation of Animax ointment at the time of debridement, and analgesic treatment (butorphanol tartrate 1 mg/kg p.o., s.i.d.) as needed for 18 mo before euthanasia. Survival time post-antemortem diagnosis with squamous cell carcinoma are given in Table 1. Of the two cases diagnosed at postmortem examination, one died under anesthesia before attempted surgical excision of the uropygial gland (case 1), and the other was euthanatized because of extensive ventral extension of the uropygial gland mass noted during a diagnostic workup (case 4). All neoplasms were regionally extensive, proliferative, and had an ulcerated epidermal surface (Fig. 1). Histopathology was consistent with squamous cell carcinoma in all cases and included irregular coalescing islands of neoplastic squamous epithelial cells, as well as a central core of keratin (keratin pearl) (Fig. 2). In case 4, the mass was adhered to the dorsal pelvis. No underlying disease processes were found at postmortem examination. Measurements of the affected uropygial gland–neoplasm measured at postmortem examination were 3.8 3 5 3 2.8 cm (case 2), 5.5 3 5 3 3.5 cm (case 4), and 5.5 3 4 3 4.5 cm (case 5). Measurements were not taken in the remaining two cases. Squamous cell carcinoma has been reported in multiple psittacine species, northern carmine beeeaters (Merops nubicus nubicus), and two penguins (African penguin [Spheniscus demersus] and rockhopper penguin but appears to be most common in chickens (Gallus domesticus).6,11,15,16,21,25,30 A wide variety of tissues are affected, including the skin of the head, neck, wings, chest, and uropygial gland, as well as the proximal alimentary tract, including beak, esophagus, crop, and proventriculus.15,25,30 Squamous cell carcinoma is typically locally invasive with a low incidence of metastasis.15,27,30 Reported avian uropygial gland neoplasms include adenoma, adenocarcinoma, melanoma, and squamous cell carcinoma.15,25,30,33,37 The incidence of uropygial gland neoplasia is sporadic with the exception of budgerigars (Melopsittacus undulates) which, as a species, appear to be overrepresented in incidence of neoplasia.7,16,25 Several treatment options for avian squamous cell carcinoma have been described. Surgical removal of the affected tissue has long been the treatment of choice for uropygial gland tumors, although these tumors tend to be locally invasive, making complete surgical resection difficult.15,17

RETTENMUND ET AL.—UROPYGIAL GLAND NEOPLASIA IN PENGUINS

Figure 2. Photomicrograph of a uropygial gland squamous cell carcinoma in a chinstrap penguin (case 3) demonstrating surface epidermal ulceration (arrow), gland effacement, and local tissue infiltration (asterisk) by nests of neoplastic squamous epithelial cells (hematoxylin and eosin).

Several other treatments have been attempted either alone or in conjunction with surgical removal or debulking. Use of a strontium-90 ophthalmic applicator for treatment of uropygial gland tumors has achieved good results with few side effects in a small number of birds, although surgical debulking may be needed with larger masses.23 Radiation therapy, specifically gamma ray teletherapy, has been used in birds to treat squamous cell carcinoma of the choana, oral cavity, and beak.7,17,20 However, there is some suggestion that these tumors are radioresistant.7,20 Both intralesional cisplatin and carboplatin have been used in the treatment of choanal, oral, submandibular, beak, and uropygial gland squamous cell carcinoma, usually combined with surgical debulking, radiation therapy, or both.6,7,17,20,30 Cryosurgery has been described for the treatment of squamous cell carcinomas of the oral cavity and face.6,8 Photodynamic therapy has been used to treat squamous cell carcinoma of the casque of a hornbill and flank of a cockatiel.7,39 However, neither therapy has been used for

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uropygial gland tumors. Treatment with analgesics, anti-inflammatory medications, and antibiotics for secondary bacterial infections can also be utilized for palliative care if more aggressive therapy is not warranted or desired. In this case series, flushing the uropygial gland and application of topical treatments usually alleviated clinical signs of impaction, abscessation, ulceration, fistula formation, or a combination of problems for various lengths of time. Treatment with systemic therapies was only implemented when changes in the appearance of the uropygial gland, such as abscess formation, ulceration, or the presence of malodorous debris, suggested systemic treatment might be needed or surgical debridement of tissues had been performed. Surgical debridement of the affected tissue was attempted in four cases but did not result in long-term resolution in any case. Additionally, the majority of squamous cell carcinomas were diagnosed in older animals (.10 yr old), and all but one individual had chronic (2–10 yr), recurrent uropygial gland problems including impaction, rupture, abscess formation, or a combination of conditions. In multiple cases where the confirmatory diagnosis was determined late in the disease process, the neoplasm may have been present for a longer duration than recognized. Over the last 13 yr, a total of 104 gentoo and chinstrap penguins greater than 2 yr of age, were in the Wildlife Conservation Society’s Central Park Zoo penguin collection, of which 28 (27%) had uropygial gland disease. Of those with disease, 17 had episodes of impacted uropgyial glands with no biopsies performed, 6 (gentoo n ¼ 2, chinstrap n ¼ 4) had histologically confirmed uropygial gland disease, ranging from impaction with cellulitis to adenitis and squamous metaplasia, and the remaining 5 (gentoo n ¼ 2, chinstrap n ¼ 3) cases had histologically confirmed squamous cell carcinoma. The underlying cause of uropygial gland disease was not clear. It could be related to altered preening behavior if birds are not emptying the gland regularly, which might occur if birds were not swimming regularly or for other social or behavioral reasons, leading to gland stasis and accumulation of glandular material and predisposing these birds to impaction and adenitis. Another possible cause is hypovitaminosis A, which has been associated with squamous metaplasia of various tissues.19 However, this seems unlikely because the birds were fed a whole-fish diet, although vitamin A levels were not evaluated in these cases. Chronic inflammation can promote neoplastic transformation of tissues in mice, and

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cancer and inflammation have been linked in human medicine.4,24,28 Therefore, it is possible that chronic uropygial gland adenitis predisposed or promoted the development of neoplasia in the affected penguins, which would suggest that aggressive treatment early in the disease process is warranted. Another factor that can contribute to the development of multicentric squamous cell carcinoma in mammals is prolonged exposure to ultraviolet (UV) light. These penguins were housed in an indoor exhibit, so excess UV light exposure is unlikely.1 Definitive treatment was not attempted in four cases because of the severity of disease, but palliative treatment was provided. In one case, removal of the uropygial gland was attempted without a confirmatory diagnosis of squamous cell carcinoma, but this animal died under anesthesia before the attempted surgical excision. Uropygial gland removal has been performed successfully in three gentoo penguins, with the only complications noted related to wound healing. Postoperative follow-up times ranged from 190 to 262 days postoperatively, and no mention was made of feather quality after surgery in these cases.18 However, the uropygial gland has important functions related to maintaining feather quality and integrity, which may be lost with the removal of the uropygial gland. Twenty-one cases of neoplasia have been reported in penguins, including 2 reports of cholangiocarcinoma,32,36 13 reports of malignant melanoma,5,14,29,37 and 1 report each of malignant lymphoma,34 lymphocytic sarcoma–mixed cell lymphoma,31 proventricular adenocarcinoma,42 gizzard adenocarcinoma,2 choanal squamous cell carcinoma,6 and uropygial gland squamous cell carcinoma.21 These limited reports of neoplasia in captive penguins and no reports of neoplasia in free-ranging penguins could reflect a low incidence of neoplasia in this species or a lack of reporting of neoplastic lesions, especially in wild birds; for the captive penguins, a small captive population limits the sample size. Incidence of neoplasia as a cause of mortality in penguins appears to be low based on the penguin species survival plan mortality report from 2007 to 2012, and no cases of uropygial gland neoplasia have been reported at other institutions during this interval (Allison Wack, pers. comm.). The prevalence of uropygial gland squamous cell carcinoma in penguin species is unknown; however, based upon the frequency observed in this penguin colony, uropygial gland neoplasia may be more common than previously recognized.

Acknowledgments: The authors thank the additional pathologists, Drs. D. McAloose and Carlos Rodriguez, who provided diagnostic support in this case series, as well as veterinary technician Berni Leahy and the Central Park Zoo animal keepers, especially the penguin staff, for their assistance and Dr. Ashleigh Walker for her preliminary Wildlife Conservation Society research on this topic.

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Uropygial gland squamous cell carcinoma in chinstrap (Pygoscelis antarcticus) and gentoo (Pygoscelis papua) penguins at the Wildlife Conservation Society's Central Park Zoo.

Uropygial, or preen, glands are found in a variety of avian species including penguins. These glands have a multitude of functions and can develop a v...
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