A CUTANEOUS RED PIGMENTED TUMOR (ERYTHROPHOROMA) W I T H METASTASES I N A FLATFISH
(PSEUDOPLEURONECTES AMERICANUS)
GEORGE MILTON SMITH
(From the Department of Anatomy, Y n f e University, Bchool of Medicine)
1
Particular interest is attached to cutaneous tumors of fishes because
of the variety of pigment cells from which such growths may have their
origin. The pigmented cells of the corium of fishes are usually grouped
as melanophores, xanthophores, erythrophores, and guanophores or
iridocytes. The normal morphology of these cells has been extensively
studied by many investigators, including Rallowitz ( l ) ,Becher (2),
Schnackenbeck ( 3 ) , Jost (4), Panu ( 5 ) , Graupner and Fischer (6).
Pigmented tumors of fishes are not uncommon. Of these, the variety most frequently seen is the melanotic type studied by Takahashi
(7), Thomas (8), Johnstone (9), Haddow and Blake ( l o ) , and others.
I n this connection it is noteworthy that Haiissler (ll),Kosswig (12),
and Gordon and Reed (13) have encountered melanotic invasive
growths experimentally in hybrids of the Mexican killifish.
A tumor containing yellow green pigment together with crystals
(allophor sarcoma) is described by Takahashi (7). The same author
found another iridescent tumor called guanophoroma in a specimen of
Hezogramm otakii. Through his studies information regarding the
physical characteristics of crystals in fish tumors has been gained.
To date only a few red pigmented fish tumors have been studied.
Thomas (8) has described three specimens designated by him as erythrophoroma, all in fishes inhabiting European waters. The first of
these, in a tunny, was a subperitoneal tumor near the esophagus, of a
mandarin color, with a metastatic nodule in the liver. The other two
were in specimens of trout, metastasis occurring in one of these.
Kosswig (14) describes two instances of localized red tumors caused
by over-production of cells containing lipochrome substances. These
were observed in cross-breeding experiments between Platypoecilus
macdatus and Xiphophorzis helleri. The red pigmented tumor reported below occurred in a sult-water fish inhabiting American waters.
This particular fish showed in the normal skin no bright red or vermilion colored chromatophores ; but here and there orange colored
pigment cells of the corium possessed a distinct reddish tinge.
Generally speaking, fish tumors remain localized. Although they
may be invasive, they rarely exhibit secondary growths. Haddow and
Blake (10) have explained this anatomically on the basis that the lymphatic system of the fish is merely a diffuse arrangement of capillaries
and spaces possessing no organized lymphatic glands. The widespread
1
Aided by a graiit from the Blossom Fund, Yale University.
596
PLATE
I
I
4
7
F I Q S . 1 AND 8. I’RIMARY ClITANEOUS ~ ‘ U i V O R AND S K I N METASTASESON P I Q N E N T E D
UPPERSURFACE
OF FLATFISH
FIG.3. CROSS-SECTIONOF MAIN TUMORNEARE E Q I O N OF RIGHT OVARY
FIGS.
4 AND 5. LIVERWITH RED COLORED
METASTASES
EXPOSED
BY REMOVAL
OF PART
OF
THE UNDEROR UNPIQMENTED SIJRPAACE
OF SKIN
There art3 two minute skin metastases iwnr the tail.
FIG.6. SPLEEN
WITH METASTASES
FIQ. 7. KIDNEY
WITH METASTASES,PERITONEITN P A R T L Y REMOVED FROM SURFACE OF
KIDNEY
1
A CUTANEOUS TUMOR IN A FLATFISH
597
metastases in the liver, spleen, kidney, and skin of the red pigmented
tumor herewith described furnishes, therefore, an example of a metastasizing fish tumor, and gives added evidence that this characteristic
of malignant growths obtains for fishes as well as f o r mammals and
birds.
DESCRIPTION
OF SPECIMEN
The flatfish (Pseudoplewolzectes anaericalzns), a female, was caught
in the waters of Long Island Sound, near Port Jefferson, March 1,1933.
Its length was 21 em., its width 12 em.
The main tumor, measuring 3 em. X 2 cm., of a brilliant vermilion
color, was situated on the upper or pigmented side of the fish (Plate I,
Figs. 1 and 2 ) 4 cm. behind the right operculum and 4 cm. below the
lateral line. Its irregular surface projected t o a height of 3 mm. above
the level of the adjacent normal skin. Here and there small orange
oolored areas and small fields of black pigmented tissue were found
scattered over the papillomatous red surface. Several points of
necrotic tissue with slight hemorrhage were also observed at the surface of the mass. The black areas represented masses of normal
cutaneons melanophores with occasional fragments of scales. The
cross-section of the tumor (Plate I, Fig. 3) showed the red tumor
tissue extending down to the thin muscle in contact with the peritoneum
overlying the right ovary. Small atrophic scales existed along the
irregular periphery of the tumor.
The following secondary nodules of tumor tissue, also bright red in
color, were found: two cutaneous nodules near the posterior edge of the
tumor (Plate I, Fig. 2 ) ; two minute cutaneous nodules in the lower or
white surface of the skin 4 em. from the base of the tail (Plate I, Fig.
4); ten nodules in the liver, five appearing along the upper surface
(Plate I, Fig. 5 ) and the remainder in the substance of the liver near
the under surface. The spleen was very largely replaced by three red
masses of tumor tissue (Plate I, Fig. G ) , the largest of which measured
12 X 8 mm. The kidney showed ten red nodules partly embedded in
renal tissue with free surfaces in contact with the peritoneum (Plate I,
Fig. 7). All secondary nodules were circumscribed and, when sectioned, showed throughout a brilliant vermilion color.
Microscopically, the primary cutaneous tumor at its surface was
necrotic in places. Musses of spindle-shaped cells (Plate 11, Fig. 1)
supported by delicate capillaries extended throughout the thickened
corium as f a r as underlying muscle bundles.
The fusif orm cells, varying in size, were usually loosely arranged,
at times rather closely packed together. Some tumor cells possessed
short processes. Frozen sections of fresh tumor tissues at the time
of death (Plate 11, Fig. 2 ) showed small pigment granules, usually
varying in color from vermilion to orange, occupying many of the cells,
These granules were concentrated especially around a large oval
nucleus. At times cells contained some very dark red and a few black
PLATE
I1
FIG.1. SECTION
OF CORIUMFROM PRIMARY
CUTANFAXISTUMOR;
PARTOF SCALE
AT POINT
A.
X 60
TISSUEFROM S K I N
FIG. 2. FROZEN SECTION OF FRESH
WITH HEMATOXYLIN
ONLY.
X 435
TUMOR,NUCLEI
STAINED LIQHTLY
Cytoplasm of spindle-shaped cells wa8 of an orange color. Cells A, B, and C contain
granules of red pigment which photograph black.
AND EOBIN).
FIG. 3. PARAFFIN SECTION OF PRIMARY CUTANEOUS TUMOR(HEMATOXYLIN
x 485
Pigment of cell bodies has become dissolved in preparation of sections, leaving
or vacuolated cytoplasm.
FIG. 4. SECTION
OF METASTATIU
GROWTH( A )
BILEDUCT.x 50
698
INVADING
R
granular
LIVER
TIBRUE (B) N U S&fatc
A CUTANEOUS TTTMOR IN A FLATFISH
599
pigment granules, mingled with the brighter red and orange. Here
and there reddish or orange colored pigment detritus was found between tumor cells. Some large mononuclear phagocytic cells filled with
red pigment were scattered in the sections, usually in small groups.
As expected, paraffin sections of tumor tissues, fixed in formalin,
showed very largely a disappearance of the pigment granules leaving
the unstained sections with a diffuse orange color, and individual cells
with a vacuolated appearance of the cytoplasm (Plate 11,Fig. 3).
Normal corial melanophores were plentiful in some areas of the primary cutaneous tumor, but apparently did not exist in the visceral
metastases, Mitotic figures were present but not plentiful in all of the
tumor tissue examined. The peripheral cells of metastases in the liver
(Plate 11, Fig. 4), kidney, and spleen infiltrated the adjacent normal
cells of their respective organs. There were no metastases in the brain,
gills, or bones.
SUMMARY
A cutaneous red pigmented tumor (erythrophoroma) with wide
spread secondary growths is described, occurring in a flatfish (Pseudoplezcronectes americalzzts) from the waters of Long Island Sound.
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