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Medycyna Wet. 2011, 67 (6) 422

Opis przypadku Case report

Hepatocellular carcinoma (hepatocellular

carcino-ma) is a malicious primary epithelial hepatic tumour

originating from hepatocytes (12). It occurs in three

forms: a massive tumour of one lobe, numerous

tuber-cules covering the entire liver parenchyma, and diffuse

infiltration. Histologically, it usually has a trabecular

structure and a high mitotic rate; individual cells can

be well or poorly differentiated (6, 11). It is identified

in various species of animals, but rarely in birds. It is

the most common primary liver cancer in dogs (14).

Hepatocellular carcinoma has been reported in various

species of wild birds, such as rosy-billed duck (Netta

peposaca), red-headed duck (Aythya americana),

orange-headed ground thrust (Zoothera citrina),

black--headed pitta (Pitta sordida), budgerigar

(Melopsitta-cus undulatus), lesser flamingo (Phoeniconaias minor),

black-headed gull (Larus ridibundus), king quail

(Co-turnix chinensis), canary (Serinus canaria) and

peach--faced lovebird (Agapornis roseicollis) (9, 11, 13, 15,

18). As for domestic birds, it rarely occurs in hens but

has been more frequently reported in ducks (9). There

are no reported cases of hepatocellular adenocarcinoma

in a racing pigeon in the available literature.

Hepatocellular adenocarcinoma is very rarely treated

separately from hepatocellular carcinoma, and the only

case of such a tumour has been described in a

white--tailed deer (11). A distinguishing criterion is the

for-mation of distinct glandular ducts.

The racing pigeon (Columba livia domestica) is a bird

bred mainly for sport purposes: it participates in

com-petitions where a good physical condition and

endu-rance matter. In sunny weather, it can return from

a distance of 1,000 km within a day (4). Individual

specimens can sometimes be very valuable.

Description of the case

The owner of an 8-month-old, 270 g racing pigeon of a highly inbred line noticed that the bird had no appetite and was considerably weakened. For 7 days before the appearance of disease symptoms, the pigeon had been fed a diet consisting exclusively of carrot. After this diet, the bird showed increased thirst, and excreted diluted greenish--yellow droppings. Clinical examination revealed enlarge-ment of abdominal integuenlarge-ments with a noticeable abdominal mass just behind the breastbone comb; strong emaciation combined with muscular dystrophy; and pain, which grew more intense during digital palpation. A suspected cause was occlusion of the alimentary canal. In order to diagnose the site of occlusion in the alimentary canal, two X-ray images with a contrast medium (barium sulfate) were taken at 20-minute intervals. The images excluded any occlusion of the alimentary canal. Ultrasonographic

exa-Hepatocellular adenocarcinoma in a racing pigeon

MAGDALENA SZWEDA, TOMASZ STENZEL*, KATARZYNA PADZIOR**, ANNA KO£ODZIEJSKA***, TOMASZ MÊCIK-KRONENBERG****

Department of Pathophysiology, Forensic Veterinary Medicine and Administration,

*Department of Bird Diseases, **Department of Pathological Anatomy, ***Department of Clinical Diagnostics of the Faculty of Veterinary Medicine of the University of Warmia and Mazury, Oczapowskiego Str. 13-14, 10-719 Olsztyn

****Department of Pathology, Medical University of Silesia, 3 Maja Str. 13-15, 41-800 Zabrze, Poland

Szweda M., Stenzel T., PaŸdzior K., Ko³odziejska A., Mêcik-Kronenberg T.

Hepatocellular adenocarcinoma in a racing pigeon

Summary

Primary hepatic tumours are rare in birds. The aim of this paper is to present a case of hepatocellular adenocarcinoma (hepatocellular adenocarcinoma) in an 8-month-old racing pigeon. Dominant symptoms in clinical examinations included lack of appetite, dyspnoea and apathy. Physical examinations revealed a perceptible mass in the anterior part of the visceral cavity. Moreover, radiological examination revealed asymmetric enlargement of the liver and the presence of fluid in the visceral cavity. Ultrasonographic exami-nation confirmed multifocal lesions in the liver tissue. Histopathological examiexami-nation of the liver revealed tumour cells forming into glandular ducts, with malignant properties and a moderate level of diversification. No description of hepatocellular adenocarcinoma in a racing pigeon has been found in the available litera-ture.

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Medycyna Wet. 2011, 67 (6) 423

mination revealed disseminated hypoechogenic lesions of the liver tissue. An X-ray examination of the visceral cavity revealed that the entire liver was enlarged, with round edges, while the image of other organs was blurred because of the accumulation of fluid inside. On the other hand, an X-ray examination of the lungs excluded tumour metasta-sis to this organ. A blood sample was taken from the basilic vein, and biochemical and morphological blood tests were

carried out, proving an increased activity of hepatic enzy-mes (tab. 1), as well as anaemia and leucocytosis.

The bird was kept for stationary treatment in a private veterinary practice specialising in treating ornamental birds. The treatment involved the application of preparations regenerating the liver parenchyma (Sodiazot, Columbovet – 0.5 ml/100 ml water/all day; Ideal Pills, Versele Laga – 1 pill a day) and hydrating the bird (Duphalyte, Scanvet – 0.5 ml s.c.1 × a day). In view of established problems with food digestion and poor appetite, the bird was given extra food in the form of a commercial feed for the manual breed-ing of parrot nestlbreed-ings, containbreed-ing digestive enzymes (HBD’s Avian Enzyme, Avifood). The feed was supplied manually with a probe to the crop. The treatment achieved a short-term improvement in the condition of the pigeon, but after two weeks its health worsened significantly, and in the third week of treatment, neurological deficiencies were observed (staggering gait, reeling, unnatural posture, paresis and paralysis of limbs). After consultations with

r e t e m a r a P Concenrtaiton Untis P L A 788 U/L T L A 105 U/L H D L 180 U/L T S A 528 U/L K C 173 U/L

Tab. 1. Biochemical blood test results in racing pigeon with hepatocellular adenocarcinoma

Fig. 1. Liver with nodular lesions in the pigeon (Columba

livia domestica) Fig. 2. Hepatocellular adenocarcinoma – cell nuclei revealsignificant polymorphism. Large nucleoli contain an acido-philic substance (arrows). HE stain.

Fig. 4. Blocks of neoplastic cells are surrounded with thick streaks of the fibrous connective tissue (white arrow), in which individual neoplastic cells occur. Thrombotic necrosis mar-ked with the black arrow. HE stain.

Fig. 3. Hepatocellular adenocarcinoma – lipid and protein sub-stances (arrows) depositing intracellularly. HE stain.

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Medycyna Wet. 2011, 67 (6) 424

the owner, the decision was made to euthanize the bird. An autopsy revealed ascites and an enlarged liver with light foci and tumours, ranging in size between 1 and 6 mm and in colour between white and brown. Samples of the changed liver were taken for histopathological examination. They were preserved in 10% buffered formalin, after which paraffin sections, 3-4 µm thick, were stained with hemato-xylin-eosin (HE) and PAS according to McManus. Micro-scopic examination revealed the presence of infiltrative neo-plastic tissue originating from hepatic cells (hepatocytes). The parenchyma of the tumour had a lobular-trabecular structure (without hepatic triads and central veins) with clear architectonical differentiation towards glandular ducts and abundant connective tissue assuming the shape of indivi-dual fragments of its tissue. Extensive necrotic foci were also observed, separated from the tumour parenchyma by a demarcation belt of connective tissue. Tumour cells showed moderate differentiation, with sparse mitotic figures, and were characterized by acidophilic cytoplasm subject to strong vacuolization. Cell nuclei with distinct nucleoli showed significant polymorphism, vesicular structure and irregular contours. The results of microscopic examinations of the pigeon’s liver enabled the diagnosis of moderately differentiated hepatocellular adenocarcinoma.

Discussion

The cause of this spontaneous primary liver cancer

in birds is unknown, although viral aetiologies (e.g.

polyoma virus, reovirus, herpesvirus, adenovirus) of

avian hepatic tumours have often been proposed (3).

It has been proven that the development of

hepatocel-lular carcinoma can be caused by the consumption of

cereal products contaminated with alfatoxynamins

produced by Aspergilus flavus. Aflatoxin has been

used to induce hepatic tumours in ducks (1, 16). The

processes of reconstruction occurring in a cirrhotic liver

can lead to the formation of a primary hepatocellular

cancer regardless of the aetiology of cirrhosis. Cirrhosis

and chronic hepatitis have both been shown to

pre-dispose ducks to the development of hepatocellular

carcinomas. Additionally, chronic inflammation

incre-ases the level of cytokines, which are responsible for

neoplastic transformation (5). The research indicates

that an increased level of iron associated with hepatic

cirrhosis intensifies neoplastic transformation (19).

Other risk factors include some inborn hepathopaties,

Trichomonas gallinae infection, hormonal disorders

and the presence of the hepatitis B virus in the body

(3, 8). Since pigeons usually feed on mixtures of

seeds, contamination of the seeds with alfatoxins may

be the main cause of hepatocellular carcinoma.

Doxy-cycline, an antibiotic that is often excessively applied

by pigeon breeders, may also be a significant

hepato-toxic factor.

Primary hepatic cancers most frequently develop

without any symptoms. Clinical symptoms appear late

and are not characteristic. Most often they concern the

alimentary canal (anorexia, flatulencies and

constipa-tions). Enlargement of the liver and ascites are

reve-aled in a later stadium (10). Hepatocellular

adenocar-cinoma is characterized by high metastatic potential.

However, these animal tumours metestasize less

fre-quently than might be predicted from their

histolo-gical features (17). Carcinomas often penetrate the

capsule to implant on the peritoneum. Hematogenous

metastases occur primarily in the lungs, and some

arrive in masses in relatively large vessels (7, 9). In

the case described here, despite the advanced stadium

of cancer, no metastasis was observed in the organs

examined (kidneys, lungs, spleen). The occurrence of

adenocarcinoma hepatocellulare in such a young bird

is also exceptional.

Surgery offers a chance to cure liver cancer if it

occurs as a single tumour. Thanks to the high

regene-rative capacity of the liver, a large part can be

remo-ved without detriment to the health of the animal. If

lesions are disseminated, and the condition of the

patient is poor, surgery is impossible. In typical cases,

the removal of the hepatocellular adenocarcinoma mass

Fig. 6. PAS-positive substance (arrows) surrounding the lobules. PAS staining according to McManus method Fig. 5. The tumour demonstrates pattern of fibrosis (arrows).

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Medycyna Wet. 2011, 67 (6) 425

allows the patient to survive for one year after the

surgery (11, 13). Euthanasia is often considered since

clinical signs arising from complications associated

with primary neoplasms (e.g. anorexia) or metastatic

neoplasms (e.g. depression, dyspnoea) are often severe.

References

1.Davies R. R.: Avian liver disease: etiology and pathogenesis, Semin. Avian Exot. Pet Med. 2000, 9, 115-125.

2.Fletcher O. J., Abdul-Azziz T.: Avian Histopathology. Am. Assoc. Avian Pathologists, Florida 2008.

3.Freeman K. P., Hahn K. A., Jones M. P., Petersen M. G., Toal R. L.: Unusual presentation of an Amazon parrot (Amazona species) with hepatocellular carcinoma. Avian Pathol. 1999, 28, 203-206.

4.Gabrisch K., Zwart P.: Praktyka kliniczna: Zwierzêta egzotyczne. Galaktyka, £ódŸ 2009.

5.Gesek M., Stenzel T., Szarek J., Babiñska J., Mieszczyñski T.: Cholangiocar-cinoma in cockatiels (Nymphicus hollandicus). Bull. Vet. Inst. Pu³awy 2009, 53, 445-448.

6.Kato M., Higuchi T., Orita Y., Ishikawa Y., Kadot K.: Combined hepatocel-lular carcinoma and cholangiocarcinoma in a mare. J. Comp. Path. 1997, 116, 409-413.

7.Kennedy F. A., Sattler A. S., Mahler J. R., Jansson P. C.: Oropharyngeal and cloacal papillomas in two macaws (Ara spp.) with neoplasia with hepatic metastastasis. J. Avian Med. Surg. 1996, 10, 89-95.

8.Kotle G. N., Bandyopadhyay A. C., Jain S. K.: Hepatocellular carcinoma in a fowl. Indian Vet. J. 1968, 7, 578-580.

9.Ling Y. S., Guo Y. J., Yang L. K.: Pathological observations of hepatic tumors in ducks. Avian Pathol. 1993, 22, 131-140.

10.Mutinelli F., Carminato A., Schiavon E., Melchiotti E., Trevisan L., Vascel-lari M.: Metastatic hepatocellular carcinoma and subcutaneous fibrosarcoma in a black-headed gull (Larus ridibundus). Vet. Rec. 2009, 164, 177-178. 11.Placke M. E., Roscoe D. E., Wyand D. S., Nielsen S. W.: Hepatocellular

ade-nocarcinoma in a white-tailed deer. Can. J. Comp. Med. 1982, 46, 198-200. 12.Reece R. L.: Observations on naturally occurring neoplasms in birds in the

state of Victoria, Australia. Avian Pathol. 1992, 21, 3-32.

13.Saif Y. M.: Diseases of Poultry. Blackwell Publishing Professional, Iowa 2003. 14.Schmidt R. E.: The avian liver in health and disease. Proc. Assoc. Avian Vet.

1999, 14, 273-289.

15.Shiga A., Shirota K., Enomoto M.: Combined hepatocellular and cholangio-cellular carcinoma in a dog. J. Vet. Med. Sci. 2001, 63, 483-486.

16.Siegfried L. M.: Neoplasms identified in free-flying birds. Avian Dis. 1983, 27, 86-99.

17.Spenser E. L.: Common infectious diseases of psittacine birds seen in practice. Vet. Clin. North. Am. (Small Anim. Pract.). 1991, 21, 1213-1230. 18.Tseng F. S.: Considerations in care for birds affected by oil spills. Semin.

Avian Exotic Pet Med. 1999, 8, 21-31.

19.Wadsworth P. F., Brancker W. M., Jones D. M.: Some hepatic neoplasms in non-domesticated birds. Avian Pathol. 1978, 4, 551-555.

20.Woods L. W., Plumlee K. H.: Avian toxicoses: Veterinary diagnostic labora-tory perspective. Semin. Avian Exotic Pet Med. 1999, 8, 32-35.

Author’s address: vet. surg. Magdalena Szweda, Oczapowskiego Str. 13, 10-719 Olsztyn, Poland; e-mail: magdalena.szweda@uwm.edu.pl

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