An Abattoir Study on Hepatic Tumors of Sheep
The aim of the present study was to assess the incidence and
age distribution of hepatic tumors of sheep as well as study of their
histopathologic characteristics. For this purpose, 3000 slaughtered sheep,
consisting of 284 rams with approximate age of 7 to 20 months and 2716
ewes with approximate age of 3 to 7 years, were inspected during a routine
postmortem examination. This study was conducted at Tabriz abattoir in
the East Azerbaijan province of Iran, in a course of 8 months from March
to November 2006. In this survey, two livers were encountered tumoral.
Representative sections of the tumors were stained with hematoxylin and
eosin. Gross and microscopic features of these tumors supported diagnosis
of hepatocellular carcinoma and cholangiocellular carcinoma for a seven-years-old
crossbreed ewe and a five-years-old native breed ewe respectively. In
this survey, 0.074% of slaughtered ewes had hepatic neoplasia. That is,
the prevalence of hepatocellular carcinoma and cholangiocellular carcinoma
in aged ewes was equally 0.037% in this study.
Hepatic neoplasms can be of epithelial or mesenchymal origin (Cullen
and Popp, 2002). These tumors tend to occur in older animals, with an
average age of 10 to 12 years (Thamm, 2001). Hepatic epithelial tumors
may arise either from the hepatic cells or from the bile ducts. The former
are called hepatomas or carcinoma hepatocellulare and the latter cholangiocellular
adenomas or carcinoma cholangiocellulare (Sundarasiva, 2002). Hepatocellular
carcinomas are uncommon in all domestic animals but occur more frequently
in ruminants, particularly sheep (MacLachlan and Cullen, 2002; Sundarasiva,
2002). This tumor has been recorded in a Holstein cow (Jeong et al.,
2005). It also has been described in a heifer (Braun et al., 1997).
Cholangiocellular carcinoma is an uncommon neoplasm of sheep (Lofstedt
et al., 1988). However, hepatocholangioma and cholangiocellular
carcinoma have been reported in sheep (Watt, 1970; Braun et al.,
1997; Lofstedt et al., 1988). Cholangioma and cholangiocarcinoma
also have been diagnosed in goats (Puette and Hafner, 1995; Rodríguez
et al., 1996). Besides, cholangioma, hepatic biliary cystadenoma,
a relatively uncommon benign tumor, has been identified in some domestic
animals, including sheep, pigs, dogs and cats (Popp, 1990; Adler and Wilson,
1995; Nyland et al., 1999). It also has been recorded in a 10-year-old
horse as the first case in Equines (Salvaggio et al., 2003). A
Combined hepatocellular carcinoma and cholangiocarcinoma has been described
in an 18-year-old Thoroughbred mare (Kato et al., 1997). It has
been revealed that hepatic and biliary neoplasms account for 10% of all
neoplasms in cattle and 31% in sheep (Anderson and Sandison, 1967). Information
from abattoir by these authors (Anderson and Sandison, 1967) indicates
that hepatocellular and biliary neoplasms are 4 times more common in cattle
than sheep. It also has been reported that 80% of hepatocellular tumors
in cattle are carcinomas (Bettini and Marcato, 1992). Primary hepatic
neoplasms are rarely seen in dogs, accounting for only 0.6 to 1.3% of
all canine neoplasms (Magne and Withrow, 1985). Results from another study
indicate that hepatocellular carcinomas are more common in dogs than cholangiocellular
tumors (Patnaik et al., 1980). A combined hepatocellular and cholangiocellular
carcinoma has been diagnosed in a 12-year-old male Yorkshire terrier dog
though; this primary hepatic tumor is extremely rare in dogs (Shiga et
al., 2001). It also has been revealed that hepatocellular carcinoma
is a common cause of morbidity and mortality in captive prairie dogs (Garner
et al., 2004). Frequency of different types of hepatic neoplasms
in cats varies from that seen in dogs and human beings, but the morphologic
features are comparable (Patnaik, 1992). There are relatively few reports
on bovine and sheep hepatic tumors at all (Kithier et al., 1974).
However, this abattoir study represents the incidence data of primary
hepatic neoplasms in sheep. We also describe the gross and histopathologic
findings of the tumors.
MATERIALS AND METHODS
For determining the incidence and age distribution of hepatic tumors
of sheep as well as study of their histopathologic characteristics, 3000
slaughtered sheep, consisting of 284 rams with approximate age of 7 to
20 months and 2716 ewes with approximate age of 3 to 7 years, were inspected
during a routine postmortem examination at Tabriz abattoir in the East
Azerbaijan province of Iran, in a course of 8 months from March to November
2006. The age and sex of these animals were recorded simultaneously. Among
these slaughtered animals, grossly, on external and cut surface observations,
two livers were encountered tumoral. For identification of these tumors
histopathologically, representative sections of the tumors were fixed
immediately in 10% neutral buffered formalin, processed routinely and
embedded in paraffin. Tissue sections were cut to 4 μm thickness
and stained with hematoxylin and eosin (Lee and Luna, 1968).
One of these livers belonged to a seven-years-old crossbreed ewe.
The sheep was of normal appearance at the time of slaughter, without any
preexisting medical conditions. At postmortem examination, a single well-demarcated
large neoplasm that had involved contiguous liver lobes was encountered.
Its diameter was recorded (D1: 23 and D2: 45 mm). On cut surface tumor
mass had been subdivided into lobules by multiple fibrous brands and the
general appearance of neoplastic mass was light tan to yellow with dark
red areas of hemorrhage (Fig. 1). Hepatic lymph node
was enlarged and hemorrhagic, with a white-gray nodule on its surface.
The lungs and other tissue and organs at the vicinity of the affected
liver, appeared grossly normal. In the affected liver, microscopically,
aggregates of neoplastic cells were seen as crude acini with scant connective
tissue stroma between them. Invasion of malignant cells at the margin
of the compressed normal hepatocytes was indicator of malignancy (Fig.
2). In higher magnification, pleomorphic
||Massive hepatocellular carcinoma; sheep. Tumor mass
is well demarcated and has been subdivided into lobules by multiple
||Low power magnification of hepatocellular carcinoma;
sheep. Aggregates of neoplastic cells are seen as crude acini (arrowheads).
Invasion of malignant cells at the margin of the compressed normal
hepatocytes (arrows) is present (H and Ex60)
cells, mitotic figures and bizarre forms were more often (Fig.
3). Besides, macroscopic and microscopic characteristics of the lesion
in the hepatic lymph node were in agreement with metastasis to it. These
findings suggest a poorly differentiated adenoid hepatocellular carcinoma
in the ewe.
Another case belonged to a five-year-old native breed slaughtered ewe
so, with the signs of unthriftiness and cachexia. Postmortem inspection
of the carcasses revealed rounded shaped, multiple firm often umblicated
pale grayish colored small-sized (8 mm in greatest diameter) nodules which
scattered randomly throughout the liver (Fig. 4). Infrequently
masses of coalescing small
||High power magnification of hepatocellular
carcinoma; sheep. Atypical hepatocytes and bizarre forms (arrows)
are seen. Mitotic figures (arrowheads) are numerous (H and E x400)
||Cholangiocellular carcinoma; sheep. Multiple raised
pale gray nodules with a central depression are present within the
nodules were observed. The same nodules were confirmed in the lungs,
also. Inspection of other tissue and organs were grossly normal. Microscopic
examinations of the liver and lungs revealed unencapsulated well-differentiated
carcinoma in which neoplastic cells had been arranged in an acinar and
tubular pattern and retained a resemblance to biliary epithelium. Scanty
connective tissue stroma existed between acini (Fig. 5).
Higher magnification showed acini lined by tall cuboidal epithelium with
infrequent papillary projections. The nuclear crowding and occasional
nests of epithelial cells in the stroma were seen. Mitotic figures were
numerous (Fig. 6). Pathologic gross and microscopic features
of this neoplasia support a diagnosis of cholangiocellular carcinoma.
||Low power magnification of cholangiocellular carcinoma;
sheep. Neoplastic cells have been organized into a tubular or acinar
arrangement (arrows) and retained a resemblance to biliary epithelium
(H and E x100)
||Cholangiocellular carcinoma; sheep. Higher magnification
shows papillary projections (arrows). Mitotic figures (arrowheads)
are numerous (H and E x400)
In this limited study the incidence data, macroscopic and then microscopic
features of the hepatocellular carcinoma and cholangiocellular carcinoma
as the most important hepatic tumors in sheep, was described. The histological
appearance of hepatocellular carcinomas varies considerably, depending
on the degree of differentiation of the individual hepatocytes and the
histological arrangement of the cells. The three major diagnostic categories
of hepatocellular carcinomas are trabecular, adenoid, and solid (Cullen
and Popp, 2002). Althothe trabecular pattern is the most common histological
form of the tumor in domestic animals (Patnaik et al., 1981) adenoid
pattern has been recognized in this survey. Based on this abattoir survey,
we propose that the primary hepatic neoplasms can be found occasionally
in sheep, although they are comparatively rare and relatively common in
old females (0.037% for each of them). In the fact, the precise incidence
of these hepatic tumors is unclear because the incidence data reported
are, based on a selected population specially, from a small geographic
area. Comparison of the incidence of these neoplasms in this study is
unreliable for similar reasons. Since, the data from this study have been
derived from an abattoir survey and relatively few animals at the earlier
stages of their life expectancy have been studied, creates another challenge
in estimating the real tumors incidences. Because of failure in getting
a precise history of the affected animals, it is not known if the incidence
of these tumors depends on some predisposing factors. In any way, the
results of this study may be in contradictory with other information,
but it seems that the incidences of neoplastic diseases are alarming on
the rise. Although, these tumors do not have a recognized cause in domestic
animals, however, various chemical carcinogens, naturally occurring carcinogens
and chronic viral, bacterial and parasitic infections may play a role
in liver cancer in domestic animals (Cullen and Popp, 2002). Therefore,
it is strongly recommended that to perform other comprehensive studies
in this connection.
The research presented in this paper was supported by
Islamic Azad University Tabriz Branch, in 2006. We wish to thank the laboratory
coworkers for preparing the pathologic sections and veterinary meat inspectors,
who collected the materials.
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