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Source: Journal of Wildlife Diseases, 12(2):167-171.
Published By: Wildlife Disease Association

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Journal of Wildlife Diseases Vol. 12, April, 1976 167


IN Mustelus canism

R. E. WOLKE, Marine Pathology Laboratory, University of Rhode Island, Kingston,

Rhode Island 02894, USA.

R. A. MURCHELANO, National Marine Fisheries Service, Middle Atlantic Coastal Fisheries

center, Pathobiology Investigations, Oxford, Maryland 21654, USA.

Abstract: A white,
raised mass present on the caudal fin of a smooth dogfish shark
(Mustelus was identified as an epidermal papilloma with areas suggestive of
carcinoma in situ. When examined by electron microscopy no structures or particles
of viral origin were apparent.

INTRODUCTION hematoxylin and eosin. Special stains in-

cluded Mallory Trichrome, Feulgen and
Neoplasms of fish are well recognized
PAS methods.
entities.216 Tumors have been reported
Tissue for electron microscopic exam-
in both the cartilaginous (Chondrichthyes,
ination was obtained by deparaffinizing
elasmobranchs) and bony (Osteichthyes,
material embedded for light microscopy
teleosts) fishes. Neoplasms appear to be
and re-embedding in Epon.
more frequent and varied in teleosts than
in elasmobranchs. Mesenchymal tumors, Sections of the tumor were submitted
to the Registry for Tumors of Lower
especially melanosarcomas, are more fre-
Animals, Smithsonian Institution, Wash-
quent among the elasmobranchs than
those of epithelial origin.0 While epider- ington, D.C.
mal papillomas frequently occur in the
higher fishes, no tumors of this type have RESULTS
been reported in the elasmobranchs.
Gross Pathology
The purpose of this paper is to describe
an epidermal papilloma of the smooth A number of white, raised, umbilicated,
dogfish (Mustelus canis) with areas sug- rough surfaced excrescences were present
gestive of carcinoma in situ. on the right lateral aspect of the caudal
fin. These masses were singular or in
groups of five or six, randomly distribu-
MATERIALS AND METHODS ted, circular, and varied in diameter from
two to 10 mm (Fig. 1). On cut surface,
A 94 cm smooth dogfish shark was
the tissue was white in color.
captured by 3/4 Yankee Otter trawl off-
shore of Cape Hatteras, North Carolina
(lat. 36#{176}08,long. 75#{176}36), 25 April Histopathology
1974. The normal epidermis of the smooth
Tissue for light microscopic examina- dogfish is composed of a non-keratinized
tion was fixed in 10% seawater formalin, stratified squamous epithelium overlying
embedded in paraffin and sectioned at 6 the base and sides of dentinal placoid
m. Sections were routinely stained with scales (Fig. 2). The epidermis is quite

rn Contribution No. 1623 of the Rhode Island Agricultural Experiment Station. Supported in part
by Sea Grant funds at the University of Rhode Island.
168 Journal of Wildlife Diseases Vol. 12, April, 1976

thin (3 to 7 cells) and contains unicel- or four layers of cells which had large,
lular mucous glands. Distinct strata simi- paler-staining, ovoid, nuclei and poorly
lar to those present in homeothermic ver- outlined cytoplasm. Overlying cells were
tebrates are not apparent; however, a irregular in orientation and had round to
basal cell layer lying immediately adja- ovoid basophilic nuclei. Outer layers were
cent to the scale or dermis is present. composed of squamous cells lying paral-
Cells within this layer are ovoid to poly- lel to the outer surface. The cytoplasm
gonal, contain large vesicular nuclei, a was often vacuolated and the nuclei deep-
single nucleolus, and a frequently vacuo- ly chromatic. Cell borders were distinct
lated cytoplasm. Their long axis lies at and intercellular bridges present resulted
right angles to the underlying dermis or in cells resembling the prickle cells of
scale. Scattered within the basal layer higher vertebrate stratum germanitivum.
and between the layer and the dermis are Mitotic figures were rare in all the cell
occasional groups of melanin-containing layers.
cells. Overlying the basal cells are layers A focus of dysplasia suggestive of car-
of irregularly-arranged polygonal epithe- cinoma in situ was present in one section
hal cells with homogeneous, non-vacuola- (Fig. 4). The focus involved the outer
ted cytoplasm and smaller, deeply baso- most cell layers and was composed of a
philic nuclei. number of anaplastic cells with large,
In areas of tumor growth, the epider- pleomorphic nuclei.
mis surrounded scales and was greatly Electron microscopic examination of
thickened due to extensive hyperplasia the tumor revealed essentially normal epi-
of the epithehial cells (Fig. 2). The thelial cells. No inclusions or viral par-
hyperplastic epidermis overlaid thickened ticles were seen.
connective tissue papillae which gave
the tumor its papillary configuration. Oc-
casional foci of mononuclear inflamma-
tory cells were present within the dermis. The papilloma is a benign tumor of
The tumor was not pedunculated but had epithehial cells which is frequently ob-
a broad base of attachment. Small blood served in homeothermic vertebrates. In
vessels were often present at the distal poikilothermic vertebrates, its prevalence
aspects of the finger-like projections (Fig. is high among the bony fishes.#{176}It is of
3). interest to note the low prevalence of epi-
Cells of the basal layer had their long thehial tumors affecting cartilagenous
axis at right angles to the connective tis- fishes and the apparent, heretofore, com-
sue papillae or the distal blood vessel. plete absence of reported papillomas in
These cells, however, tended to have lar- this group. It is doubtful that this pre-
ger, denser nuclei and a non-vacuolated valence accurately reflects actual occur-
cytoplasm when compared to similar cells rence. More likely it is related to the few
from normal epidermis. This long-axis careful post-mortem examinations con-
orientation continued into the next three ducted on these animals. Nonetheless,

1. Multiple, umbilicated, raised papillomatous masses on skin.

2. Section through caudal fin with papilloma at top of picture and normal epidermis at
bottom. Note hyperplastic epithelium overlying thickened connective tissue papillae.
X100 H + E.

3. Vascularized projection of hyperplastic epidermis. Note basal layer epithelial cells have
dense nuclei, and pale, sparse cytoplasm and are oriented at right angles to blood vessel.
X400 H + E.

4. Focus of dysplasia suggestive of carcinoma in situ. Periphery of tumor at left. Underlying

cells are anaplastic with highly pleomorphic nuclei. X400 H + E.
Journal of Wildlife Diseases Vol. 12, April, 1976 169

- C -
170 Journal of Wildlife Diseases Vol. 12, April, 1976

one must consider the possibility that all three appear as raised white areas on
there may be something unique about the skin surface. The papilloma, however,
these fishes which results in a lowered was composed of discreet, round foci and
prevalence of neoplasia. its surface was umbilicated. Epidermah
As one descends the phylogenetic scale, hyperplasia and fish pox are not so fo-
the histopathologic characteristics of the cally discreet or round and their surfaces
papilloma (i.e. thickened epithelium, ir- are smooth, resembling a whitish, wax-
regular dermal papillae) are common to like material.
many species. These same characteristics Histologically, the papilloma consisted
were present in the elasmobranch papil- of more than simple epidermal hyperpla-
loma. It is tempting to hypothesize that sia. The dermis was thickened, thrown
the similarities among species might ex- into finger-like projections and had focal
tend beyond histological appearance and
areas of mononuclear inflammation.
include etiology as well. Papillomas of
reports no visible effect on the
man and many domestic animals are of
dermis in epidermal hyperplasia and
viral origin. Wellings et al. in 196510 re-
Mawdesley-Thomas and Bucke5 and
ported virus-like particles within papil-
Lucky make a similar observation for
loma epidermal cells of the flathead sole
(Hippoglossoides elassadon).
fish pox.
Perhaps the most striking characteristic
Similarly, a condition known as epi-
dermal hyperplasia of freshwater fish has of this tumor is the focus of dysplasia
been reported in Penca flasescens, Lepo-
suggestive of carcinoma iii situ. There can
mis mnacroc/iirus and Stizostedion vii- be littlequestion that the cells in this area
reum. In the latter fish, virus particles are irregular, regressive, pleomorphic and
were seen with electron microscopy.6-#{176} dysplastic. Such a focus in a mammal
This epidermal hyperplasia resembles so- would warrant a guarded prognosis and a
called fish pox of European cyprinids. probable diagnosis of carcinoma in situ.
which is also thought to be of viral eti- Only one malignant tumor, other than the
ology.5 Electron micrographs of shark questionable report of Stolk7 has been re-
papilloma epidermal cells revealed no ported in an elasmobranch. This tumor, a
particles or structures that might be con- splenic reticulum cell sarcoma, was sub-
strued as viral. However, it should be mitted by OGara and Ohiverio to the
pointed out that the material was initial- Registry of Tumors in Lower Animals,
ly fixed in 10% formalin and re-embed- Smithsonian Institution, Washington, DC
ded in Epon. While micrographs appeared (RTLA 523). It is unfortunate that the
to be of good quality and resolution, sharks hazardous environment gives little
masking artifacts may have been present. chance for the debilitated animal to sur-
There are some gross and histologic vive. Observations of the prevalence and
similarities among the papilloma reported biologic activity of neoplastic processes in
here and the epidermal hyperplasias and/ these animals are difficult for the fish
or fish pox of freshwater fish. Grossly, pathologist to acquire.


We wish to thank Mr. John Ziskowski of the N.M.F.S.. Middle Atlantic Coastal Center, Sandy
Hook Marine Laboratory, Highlands, New Jersey for collection of the specimen.


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Journal of Wildlife Diseases Vol. 12, April, 1976 171

3. LUCKY, Z. 1970. Pathological changes with pox (Epithehioma papulosum) in

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Received for publication 4 August 1975