TUMORS I N CAPTIVE PRIMATES WITH A DESCRIPTION OF A GIANT CELL TUMOR I N A CHACMA
BABOON, PAPIO PORCARI US
HERBERT L. RATCLIFFE
(From the Laboratory oj Comparative Pathology of the Philadelphia Zoological Society,
and the McManes Laborntory oj Pathology of fhe Univertrity oj Pennsyluunia)
The occurrence of tumors in captive wild animals is by no
means uncommon. About two per cent of over five thousand
birds and mammals autopsied at the Philadelphia Zoological
Garden have been found to be affected (Fox, 1923) (1). A
comparable incidence has also been reported from animals dying
in the London Zoo (Proc. Zool. Soc. London, 1908-1929), and
interesting single cases are described from other collections.
There is, however, considerable variation in the extent to
which the different zoological groups, represented in the material
collected at the Philadelphia Zoo, are affected. For instance,
rodents, carnivora and marsupials have a relatively high tumor
incidence-more than four per cent-while in seven hundred
only five tumors have been
and seventeen autopsies on
found. No analysis of autopsy records of the London Gardens
is available, but, because of the larger size of their collection, it
seems safe to assume that their primate material must be a t
least as extensive as in Philadelphia. Yet only two tumors
have been reported. These are described as "a Sarcoma of a
scalp in a Cercopitheque " and "an adeno-sarcoma in the kidney
of an Ouakari" (Plimmer, 1914, 1915) (2).
Two of the five cases found in the Philadelphia Garden occurred in animals dying of other disease. One was a papillary
adenoma of the gastric mucosa in an Hamandryas baboon,
Papio hamandryas, and the second a hypernephroma in a brown
cebus, Cebusfatuellus. In the other three cases, the tumors were
of primary importance in the deaths of the animals. The first
of these was an adeno-carcinoma of the rectum of a Toque ma453
30
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HERBERT L. RATCLIFFE
caque, Macacus pileatus. There was extension to the prostate,
and death was apparently due to hemorrhages from the cancer.
The second of these cases was also an adeno-carcinoma. This
involved the head of the pancreas in a Grivet monkey, Cercopithecus sabaeus, and death was due to acute pancreatitis and
enteritis. The third of this series, a giant cell tumor, occurred
in a Chacma baboon, Papio porcarius. This case presents several interesting considerations and is reported here in detail.
According to the keeper the tumor was first noticed on
July 25, 1929, as a small ulcerated swelling on the back of the
right wrist near the outer margin. The swelling and ulceration
continued so that about two weeks later the animal was transferred from the exhibition house to the quarantine room of the
laboratory.
When first seen by the writer, the growth was a fairly firm,
irregular mass, six to seven centimeters across, with rounded
edges rising one to two centimeters above the surrounding tissue
and occupying much of the dorsal and lateral surface of the hand
and wrist. The epidermis had sloughed away over most of the
surface, leaving it bare and ulcerated, or covered by a black
crust. On the upper lateral edge of the mass just over the
head of the ulna there was an ulcer, about two centimeters
TUMORS I N CAPTIVE PRIMATES
455
across, from which a piece of tendon protruded and a t the base
of which the bone could be seen. (Figure 1 is a photograph of
the tumor taken at this time.)
-4few days later (September 9th) a biopsy was done, a small
piece of tissue being removed near the upper edge of the tumor.
The following is a description of a section from the biopsy specimen :The tissue is made up'of a loose stroma, numerous thin-walled
capillaries, and large numbers of giant cells. The stroma is
composed of large spindle cells, gigantic cells and, apparently,
some of the giant cells are included, or, at least, intimately
associated with the other elements. The other giant cells lie
free in spaces in the stroma. There are cells present which
seem to be intermediate between the so-called gigantic cells
which have a single, large, irregular hyperchromatic nucleus, and
the giant cells with varying numbers of small, oval, vesicular
nuclei scattered throughout the cytoplasm. These apparently
intermediate cells have both the small and large nuclei within a
single cell. Other cells seem to be intermediate between the
large spindle cells and the gigantic cells, both in size and character of their nuclei.
456
HERBERT L. RATCLIFFE
The histology of the tumor, as seen in the biopsy section,
appears most nearly comparable to that of the giant cell tumor
of man, but the tumor is hardly typical either grossly or microscopically. However, these differences will be discussed after
other features of the case have been described.
Four weeks after the biopsy was done, the animal was chloroformed. He had become progressively weaker, ate little, and
lost considerable blood through self-inflicted injuries to the
tumor. During this time the growth had not increased greatly
in size, but became infested with fly larvae about the last week
of life.
At autopsy metastases were found in the lungs, right ventricular wall and right gluteus muscles. In the lungs there were
eight small, firm nodules 0.2 to one centimeter in diameter developing near the lateral margins. These were greyish white on
section and loosely embedded in the lung parenchyma. The
metastasis to the heart was found apparently growing from the
ventricular septum just under the tricuspid valve. I t was a
cylindrical growth about 0.5 centimeter in cross section and one
centimeter in length, with a small thrombus forming on the
exposed end. The secondary growt,h in the gluteus muscles was
quite large, measuring four to five centimeters across.
TUMORS I N CAPTIVE PRIMATES
457
The original growth was somewhat changed. The fly larvae
had penetrated deeply into the mass, removing considerable
amounts of tissue. The ulcer over the head of the ulna had
increased in size and the bone was clearly visible a t its base.
The ulna was split by saw dorsoventrally, and the section extended through the carpal region. From this it was seen that the
epiphysis was raggedly eroded, and fractured, and the joint
cavity destroyed. The tumor seemed to have begun in or near
the epiphysis, which it destroyed dorsally, then to have in-
filtrated the tissues of the carpal region distally and laterally.
There was no apparent invasion of the bones and no evident
periosteal reaction along the line of section. I n other areas,
where ulcerations and erosions had penetrated to the periosteum,
it appeared thickened and there were heavy fibrous outgrowths.
These probably represent more the results of secondary infection and irritation by fly larvae than reaction to the tumor
growth.
Sections taken a t autopsy, from the tumor and metastases,
show essentially the same histology as was seen in the biopsy
specimen. Sections from points in the original growth near
areas of suppuration show considerable increase in the fibrous
458
HERBERT L. RATCLIFFE
stroma, and in vascularity. The giant and gigantic cells are
always present. However, the numbers vary considerably in
different areas. Sections from an area that had not suppurated
do not show this increase in the stroma (Fig. 2). Apparently
the growth was invasive locally. Small areas of bone and cartilage that are included in the sections seem to be invaded by
the tumor growth (Fig. 3). This feature seems further indicated
by sections from the lung and heart metastases. In the lung
giant cells were found in a bronchus near one of the secondary
nodules (Fig. 4), while in the heart these cells had penetrated
short distances into an overlying thrombus.
The histology of the lung and heart metastases is quite like
that of the biopsy specimen. In the muscle metastasis, however, there is a much more abundant stroma composed of large
and small spindle cells and occasional gigantic cells. Giant
cells in considerable numbers are scattered throughout this
tissue.
ATTEMPT AT TRANSPLANTATION
At autopsy Dr. F. D. Weidman removed two small metastatic
nodules from the lungs, macerated them in sterile salt solution,
to which a sterile suspension of cholesterol had been added, and
implanted this material on the periosteum of the scapulae of
two Rhesus macaques, Macacus rhesus. Although the transplant was done under aseptic conditions, there is no evidence,
after five months, that the experiment was successful in either
monkey.
DISCUSSION
The typical giant cell tumor of man develops within a long
bone near the end-slowly eroding the shaft and elevating the
periosteum which lays down a thin layer of bone about the developing mass. It does not ,perforate or infiltrate surrounding
tissue early and very rarely gives metastases. Histologically
it is composed of stroma and giant cells. The cells of the stroma
characteristically do not show pleomorphism (Kolodny, 1927)
(3).
I n this case the tumor developed rapidly. Probably not
longer than four or five months elapsed between the time of
TUMORS I N CAPTIVE PRIMATES
459
origin and the death of the animal. Its presence was noted
about three months before the animal was killed. It perforated
the shaft without expansion, and metastatic growths were found
at autopsy. There was marked pleomorphism in the stroma and
among the giant cells. These features, and the presence of
considerable numbers of gigantic cells, which are usually associated with osteogenic sarcoma, make it somewhat difficult to
identify as a giant cell tumor. However, S. G. Scott (1929) (4)
states that there are two general types of giant cell tumors.
First, there are those that grow slowly and produce the t,ypical
form mentioned above and, second, those that grow rapidly and
penetrate the shaft early without allowing time for the bony
capsule to be formed. Possibly the tumor described here may
be of the latter type. However, the atypical development and
histology may have been partly due to the fact that the growth
was constantly subject to irritation. The animal was continually scratching and licking the mass, and it ulcerated and became infected early in its development. I n any case, the constant presence of large numbers of giant cells in any part,s of the
tumor and in its metastases seems to indicate that it should be
classed with the giant cell tumors.
The occurrence of giant cell tumors in captive wild animals
is decidedly uncommon and those that have been reported were
not typical. H. H. Scott (1927) (5) has reported one case from
the London Zoo in which the tumor involved the heart wall of an
Indian rhinoceros. There were numerous metastases to the
lungs and pericardium, but no bones were involved. A second
case from the London Gardens was reported by Hamerton (1929)
(6). This occurred in a common fox, Vulpes vulpes, involving
the second, third and fourth left costal cartilages and giving
metastases to the lungs. With the exception of the present, no
other examples have been found in over nine thousand five hundred autopsies on wild animals dying in the Philadelphia
Gardens.
SUMMARY
The present paper describes a giant cell tumor that occurred
in a Chacma baboon, Papio porcarius, and discusses the tumor
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HERBERT L. RATCLIFFE
incidence in lower primates as compared to other captive wild
mammals. In the Chacma baboon the growth originated near
the lower epiphysis of the ulna, perforated the shaft and articular
cartilage, and infiltrated surrounding tissue. The development
was rapid, and, a t death, metastases were found in the lungs,
heart and gluteus muscles. Microscopically the tumor was
made up of a stroma composed of large spindle cells and gigantic
cells, numerous thin-walled capillttries, and large numbers of
giant cells embedded in the stroma. An attempt to transfer the
tumor to Macacus rhesus monkeys failed. Six other reports of
tumors in primates were found in available literature.
REFERENCES
(1) Fox, H.: 1923. Diseases in captive wild n ~ a n ~ m u ant1
l s birds. Lippincott,
Philadelphia, 665 pp.
Fox, H.: 1929. Some observations on comparative constitution in ]nun and
the lower animals. Proc. Amer. Phil. Soc., 68, 1: 27-51.
(2) PLIMMER,
H. G.: 1914. Report on the deaths which occurred in the Society's
Garden during the year 1913. Proc. Zool. Soc. London (1914).
PLIMMER,
H. G . : 1915, Report on the deaths which occurred in the Society's
Garden during the year 1914. Proc. Zool. Soc. London (1914).
(3) KOLODNY,
A,: 19'27. Bone sarcoma. The Surgical Publishing Co., Chicago,
214 pp.
(4) SCOTT, S. G.: 1939. Giant cell tumors of bone and their radiological diagnosis.
Proc. Roy. Soc. Med., 22, 12: 1539-1541.
(5) SCOTT,
H. H.: 1927. Neoplasm in an Indian rhinoceros (sarcoma of heart and
lungs). Proc. Zool. Soc. London (1927): 173-198.
(6) HAMERTON,
A. E.: 1929. Report on the deaths occurring in the Society's
Gardens during the year 1928. Proc. Zool. Soc. London (1929): 49-59.