Avian Pathology (1999) 28, 203±206

CASE REPORT

Unusual presentation of an Amazon parrot (Amazona species) with hepatocellular carcinoma K. P. Freeman 1 , K. A. Hahn 1 , M. P. Jones1 , M. G. Petersen 1 & R. L. Toal2 Departments of 1 Comparative Medicine and 2Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, Tennessee, 37901 1071, USA.

Non-haematopoietic hepatic malignancies are uncommon in birds. The clinical presentation (i.e. chronic buphthalmos) and non-speci® c radiographic ® ndings observed in this adult Amazon parrot (Amazona spp.) were not consistent with previous reports describing the natural behaviour of metastatic hepatocellular carcinoma in birds.

Although extremely uncommon, both primary and metastatic non-haematopoietic neoplasms have been reported to occur in the liver of birds (Sriraman et al., 1981; Aydin et al., 1991; Kennedy et al., 1996; Reece, 1996). In this case report, the clinical presentation (i.e. chronic buphthalmos) and non-speci® c radiographic ® ndings observed in an adult Amazon parrot (Amazona spp.) were not consistent with previous reports describing the natural behaviour of metastatic hepatocellular carcinoma in birds. An adult Amazon parrot (Amazona spp.) presented to the University of Tennessee Veterinary Teaching Hospital Exotic Animal Practice with an enlarged right eye. Intermittent episodes of epiphora had been noted over the previous 10 to 12 months. The bird’ s appetite remained normal; however, stools had been watery over the previous month and the bird was mildly dehydrated. An ophthalmologic examination revealed a glaucomatous eye with communication between the anterior and posterior chambers due to aspiration of aqueous humour from the posterior chamber and concomitant collapse of the cornea. A needle aspirate of the posterior chamber of the right eye was obtained and cytological examination revealed a non-diagnostic acellular sample. Radiographs of the skull showed a severe soft tissue swelling in the region of the right eye (Figure 1). Bony structures of the right orbit appeared to be normal. Due to the displaced position of the scleral bone within the eye, the impression was that the swelling was either in the posterior Received 11 March 1998. Accepted 17 August 1998 0307-9457/99/020203-04

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1999 Houghton Trust Ltd

chamber or retro-orbital in nature. A radiographic diagnosis of a possible retro-orbital mass of unknown aetiology was made. The infra-orbital sinus was aspirated and cytological examination revealed a non-diagnostic acellular sample. Bacterial culture of the conjunctiva and sinus were negative for pathogens. The bird was placed on topical antibiotics for 1 week. The ocular swelling diminished gradually, but not entirely. Fourteen months later, the eye had enlarged to where the bird was unable to close its eyelids. The cornea was intact and clear when admitted to the hospital. Radiographs of the skull demonstrated a slight orbital bony sclerosis with a major increase in the extent of the ocular protrusion, but no other evidence for a cause. An attempt was made to aspirate the retrobulbar region and in the process, the posterior chamber was entered. Elevated pressure in the posterior chamber resulted in the expression of clear liquid into the syringe. It was determined that the ¯ uid was aqueous humour and a decision was made to enucleate the eye. During the surgical procedure the bird died and a necropsy was performed. A pinkish yellow mass 0.5 3 3 cm lined the lateral portion of the orbit, and extended ventrally and dorsally, lining most of the anterior part of the orbit. The mass extended medially to the optic nerve which otherwise appeared normal. Upon examination of the abdomen and thorax, the liver was diffusely yellow tan in colour and the edges of the left liver lobes were slightly rounded.

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Figure 1. Ventrodorsal radiographs of the skull from an Amazon parrot presenting for buphthalmos and epiphora were suggestive for the presence of an intra-ocular or retrobulbar soft tissue mass.

On the cranial border of the left lateral lobe, a 0.5-cm diameter, ® rm, white nodule was observed. A similar 0.3-cm nodule was observed on the cut surface of the left lateral lobe. The spleen was enlarged (1 cm diameter) and contained a 0.5-cm diameter white nodule which was ® rmer than the surrounding spleen. The kidneys were pale brown in colour.

Histological examination revealed variable sized foci of non-encapsulated neoplastic cells throughout the liver (Figure 2). The tumour cells had vesiculated nuclei, often with one to several prominent nucleoli, and a scant to moderate amount of acidophilic or vacuolated cytoplasm, often with indistinct borders. Scattered throughout the neoplastic foci were slight to moderate numbers of lymphocytes and heterophils. The neoplastic cells were frequently arranged into either small pseudoacinar structures or into cords. The spleen, brain and lung contained neoplastic cells of similar morphology. The masses of the orbital and retrobulbar region consisted of neoplastic cells similar in appearance to those observed in the liver. The cells were often arranged in sheets or small pseudo-acinar structures with a thin ® brovascular stroma. Neoplastic cells often in® ltrated into adjacent skeletal muscle that often had muscle ® bres of varying sizes. There were a few areas of coagulation necrosis and nuclear streaming in adjacent ® brous connective tissue. Neoplastic cells had also invaded into several peripheral nerves, and into periocular glands and ducts. The neoplastic cells were pleomorphic, ranging from cells with small hyperchromatic nuclei to cells with very large nuclei often with one to several prominent nucleoli, and had amphophilic cytoplasm with indistinct borders. Diagnoses of hepatic carcinoma with metastases to the right periocular region, spleen, brain and lung was made. The large size of the ocular metastatic lesion and subsequent compression of adjacent tissues probably caused strangulation of the venous drainage from the eye resulting in the glaucomatous presentation.

Figure 2. Photomicrographs of the liver. (A) Neoplastic hepatic carcinoma cells showing pseudo-acinar structures (HE stain, bar 5 100 m m). (B) Higher magni® cation of pleomorphic hepatic carcinoma cells showing large vesiculated nuclei with one to several nucleoli (HE stain, bar 5 100 m m).

Hepatocellular carcinoma in an Amazon parrot

Although extremely uncommon, both primary and metastatic non-haematopoietic neoplasms have been reported to occur in the liver of birds (Sriraman et al., 1981; Aydin et al., 1991; Kennedy et al., 1996; Reece, 1996). The most commonly reported hepatic tumour in birds is cholangiocarcinoma, with a reported increased incidence of occurrence in Amazon parrots (Sriraman et al., 1981; Aydin et al., 1991; Reece, 1996). Other types of avian hepatic tumours that have been observed include hepatoma, haemangiosarcoma, ® brosarcoma, adenocarcinoma, hepatocellular carcinoma, biliary adenoma, hepatic lymphosarcoma and lymphoid leukosis (Aydin et al., 1991; Purvulov & Bozhkov, 1984; Reece, 1996). Among zoo birds, hepatic carcinomas have been reported in a male rosy-billed duck (Netta peposaca), a female red-headed duck (Aythya americana), a female orange-headed ground thrush (Zoothera citrina) and a female black-headed pitta (Pitta sordida) (Lombard & Witte, 1959). Two cases of carcinoma simplex of the liver were also reported in budgerigars of both sexes, with metastasis to the spleen in the female (Ratcliffe, 1933). There has been a single report of a malignant hepatoma in a pet hill mynah (Gracula religiosa), a metastasizing hepatocellular carcinoma in a lesser ¯ amingo (Phoeniconaias minor), a metastasizing bile duct carcinoma in a Chilean ¯ amingo (P. ruber chilensis) and a liver cell adenoma in a Luzon hornbill (Buceros hydrocerox hydrocerox) (Wadsworth et al., 1978; Spira, 1979). Among domestic birds, hepatocellular adenomas and carcinomas are uncommon in chickens, but more common in ducks (Rigdon & Leibovitz, 1970; Ling et al., 1993). Although uncertain, viral aetiologies (e.g. herpesvirus, polyoma virus, adenovirus, reovirus) for avian hepatic tumours have been proposed (Mladenov et al., 1979, 1980; Reece, 1996; Schaff et al., 1978). A¯ atoxin has been used to induce hepatic tumours in ducks, and many of the spontaneously occurring tumours have been associated with chronic hepatitis and cirrhosis (Sriraman et al., 1981; Dillberger et al., 1986). Chemical carcinogens (e.g. iron) have also been used to induce a variety of hepatic tumours (Dillberger et al., 1986). Cirrhosis and chronic in¯ ammation, both known to have a viral aetiology in birds, have been shown to predispose ducks and woodchucks to the development of hepatocellular carcinomas (Aydin et al., 1991; Reece, 1996). Malignant hepatic neoplasms must be differentiated from non-neoplastic conditions including hepatic nodular hyperplasia, bile duct hyperplasia and biliary cysts (Sriraman et al., 1981; Aydin et al., 1991; Beard et al., 1975; Dillberger et al., 1986; Reece, 1996). Birds with hepatocellular carcinoma frequently present in a debilitated state with enlargement of one liver lobe (McMillan, 1986).

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Abdominal enlargement may be apparent on physical examination. Hepatic epithelial tumours may arise from hepatocytes or biliary epithelium (Beard et al., 1975). Both types have been seen in birds, but tumours of the biliary system appear to be more common (Aydin et al., 1991). Some reports do not distinguish between the two. Hepatocellular carcinomas may vary in size and colour ranging from light tan to more normal red brown (Sriraman et al., 1981; Purvulov & Bozhkov, 1984). These neoplasms progressively invade surrounding hepatic tissue as neoplastic clusters rather than diffusely invade the parenchyma (Beard et al., 1975). This invasion is not uniform and may occur in sporadic areas. Vascular invasion occurs. Histological appearance is characterized by cords of hepatocyte-like cells with effacement of normal tissue architecture, bizarre to multinucleated hepatocytes and variable numbers of mitotic ® gures (Beard et al., 1975; Purvulov & Bozhkov, 1984). Metastases most often spread haematogenously and are found in the regional lymph nodes and lung (Reece, 1992). Lung metastases are characterized as small and numerous, and are found in the capillaries of the alveolar walls (Sriraman et al., 1981). Other reported sites of metastasis have included the heart, kidney, intestine, brain and ovary (Purvulov & Bozhkov, 1984). Metastasis to the peritoneum via direct extension or rupture of the tumour through the hepatic capsular surface has been observed (Purvulov & Bozhkov, 1984). Although excision (i.e. partial to full hepatic lobectomy) has been considered for the treatment of hepatic neoplasms, the prognosis is grave. Euthanasia is often considered at initial presentation, since clinical signs arising from complications associated with primary neoplasm (e.g. anorexia, cachexia) or metastatic neoplasm(s) (e.g. dyspnoea, depression, lethargy) are often severe (Aydin et al., 1991; Reece, 1996). Because the avian eye is reinforced by scleral ossicles, buphthalmos is not expected (Dukes & Pettit, 1983). In contrast, exophthalmos occurs with some frequency and usually indicates a retrobulbar space occupying lesion or extension of malignant ocular neoplasia into the retrobulbar space (Blackmore, 1966). In birds, exophthalmos has been associated with various intra-ocular neoplasms (i.e. medullo-epithelioma, rhabdomyosarcoma), retrobulbar neoplasms (i.e. lymphoma, pituitary adenoma and adenocarcinoma, undifferentiated carcinoma, teratoma) and non-neoplastic masses (i.e. abscess, cellulitis; Dukes & Pettit, 1983; Blackmore, 1966). The clinical presentation (i.e. chronic buphthalmos) and non-speci® c radiographic ® ndings observed in this adult Amazon parrot were not consistent with previous reports describing the natural behaviour of metastatic hepatocellular carcinoma in birds.

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Acknowledgements The authors thank Drs John New and Michael Walker for their management of this case. References Aydin, Y., Atasever, A. & Kokuuslu, C. (1991). Poultry diseases, including neoplasms, seen in poultry in the period 1974±1991. Veteriner Fakultesi Dergisi Universitesi Ankara, 38, 352±358. Beard, J.W., Hillman, E.A., Beard, D., Lapis, K. & Heine, U. (1975). Neoplastic response of the avian liver to host infection with strain MC29 leukosis virus. Cancer Research, 35, 1603±1627. Blackmore, D.K. (1966). The clinical approach to tumours in cage birds. I. The pathology and incidence of neoplasia in cage birds. Journal Small Animal Practice, 6, 217±223. Dillberger, J.E., Citino, S.B. & Altman, N.H. (1986). Four cases of neoplasia in captive wild birds. Avian Diseases, 31, 206±213. Dukes, T.W . & Pettit, J.R. (1983). Avian ocular neoplasia: a description of spontaneously occurring cases. Canadian Journal of Comparative M edicine, 47, 33±36. Kennedy, F.A., Sattler Augustin, S., Mahler, J.R. & Jansson, P.C. (1996). Oropharyngeal and cloacal papillomas in two macaws (Ara spp.) with neoplasia with hepatic metastasis. Journal of Avian M edicine and Surgery, 10, 89±95. Ling, Y.S., Guo, Y.J. & Yang, L.K. (1993). Pathologic observations of hepatic tumours in ducks. Avian Pathology, 22, 131±140. Lombard, L.S. & Witte, H.J. (1959). Frequency and types of tumours in mammals and birds of the Philadelphia Zoological Gardens. Cancer Research, 19, 127±141. McMillan, M.C. (1986). Radiographic diagnosis of avian abdominal disorders. Compendium of Continuing Education, 8, 616±632. Mladenov, Z., Nedyalkov, S., Ivanov, I. & Toshkov, I. (1979). Character of neoplasia in chickens inoculated with cells or cell free material from a transplantable hepatoma induced by the (avian leukosis) virus strain MC29. Obshcha i Sravnitelna Patologiya, 6, 5±23. Mladenov, Z., Nedyalkov, S., Ivanov, I. & Toshkov, I. (1980). Neoplastic growth in chickens treated with cell and cell free material from transplantable hepatoma induced by virus strain MC 29. Neoplasma, 27, 175±182. Purvulov, B. & Bozhkov, S. (1984). Pathology of some spontaneous neoplasms of fowls. Obshcha i Sravnitelna Patologiya, 16, 55±58. Ratcliffe, H.L. (1933). Incidence and nature of tumours in captive wild mammals and birds. American Journal of Cancer, 17, 116±135. Reece, R.L. (1992). Observations on naturally occurring neoplasms in birds in the state of Victoria, Australia. Avian Pathology, 21, 3±32. Reece, R.L. (1996). Some observations on naturally occurring neoplasms of domestic fowls in the State of Victoria, Australia (1977±87). Avian Pathology, 25, 407±447.

Rigdon, R.H. & Leibovitz, L. (1970). Spontaneously occurring tumours in the duck: a review of the literature and report of three cases. Avian Diseases, 14, 431±444. Schaff, Z., Talas, M., Stoger, I., Lapis, K. & Foldes, I. (1978). Neoplastic response of turkey liver to MC29 leukosis virus. Acta M orphologica Academiae Scientiarum Hungariciae, 26, 325±332. Spira, A. (1979). Hepatoma in a mynah. M odern Veterinary Practice, 60, 925±926. Sriraman, P.K., Ahmed, S.R., Naidu, N.R.G. & Rao, P.R. (1981). Neoplasia in chicken and ducks. Indian Journal of Poultry Science, 16, 436±437. Wadsworth, P.F., Majeed, S.K., Brancker, W.M. & Jones, D.M. (1978). Some hepatic neoplasms in non-domesticated birds. Avian Pathology, 7, 551±555.

REÂSUMEÂ Carcinom e heÂpatocellulaire chez un perroquet de l’ Am azone (Amazona, species) Les tumeurs heÂpatiques non heÂmatopoõ È eÂtiques sont peu freÂquentes chez les oiseaux. Les signes cliniques (c’ est-aÁ-dire buphtalmie chronique) et le observations radiographiques non speÂci® ques enregistreÂs chez ce perroquet adulte (Amazona species) n’ ont pas eÂteÂen accord avec les rapports preÂceÂdents deÂcrivant les symptoÃmes d’ un carcinome heÂpatocellulaire meÂtastasique chez les oiseaux.

ZUSAMMENFASSUNG Ein auû ergewoÈ hnlicher Fall Am azone (Amazona spp.)

von

Leberzellkrebs

bei

einer

Nicht-haÈmatopoetische Lebertumoren sind bei VoÈ geln ungewoÈ hnlich. Das klinische Bild (d.h. chronischer Buphthalmus) und die bei dieser adulten Amazone (Amazona spp.) festgestellten unspezi® schen RoÈ ntgenbefunde stimmen nicht mit den fruÈ heren Berichten uÈ berein, die das natuÈ rliche Verhalten metastasierender Leberzellkarzinome bei VoÈ geln beschreiben.

RESUME N Presentacion inusual de un carcinom a hepatocelular en una Am azona (Amazona spp.) Las neoplasias hepaÂticas malignas de origen no hematopoyeÂtico son poco frecuentes en aves. El cuadro clõ  nico (buftalmia croÂnica) y los hallazgos radiogra® cos inespecõ  ® cos observados en esta amazona (Amazona spp.) no coinciden con descripciones anteriores acerca del comportamiento y metaÂstasis de los carcinomas hepatocelulares en aves.

Unusual presentation of an Amazon parrot (Amazona species) with hepatocellular carcinoma.

Non-haematopoietic hepatic malignancies are uncommon in birds. The clinical presentation (i.e. chronic buphthalmos)and non-specific radiographic findi...
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