CONTEMPORARY TOPICS © 2005 by the American Association for Laboratory Animal Science Volume 44, No. 4 / July 2005
Mammary Ductal Carcinoma with Comedo Pattern in a
JOANNE M. SMITH, DVM, DIPLOMATE, ACLAM,1,* SRINIVAS S. RAO, DVM, PHD,2
KYLE C. STUMP, DVM, DIPLOMATE, ACLAM,3 CINZIA BENAZZI, DVM, DIPLOMATE, ECVP,4
GIUSEPPE SARLI, DVM,4 and LOUIS J. DETOLLA, VMD, PHD, DIPLOMATE, ACLAM5
NIH/OD/ORS/DVR, 9000 Rockville Pike, Bldg.14F, Rm.101, Bethesda, Maryland 208921;
NIH/NIAID/VRC, 40 Convent Drive, Rm. 1407, Bethesda, Maryland 208922;NIH/NCI
Laboratory Animal Science Program, 31 Center Drive, Bethesda, Maryland 208923;
Division of Veterinary Pathology, Department of Veterinary Public Health and Animal
Pathology, University of Bologna, Ozzano Emilia, 60066 Bologna, Italy4; University of
Maryland, School of Medicine, Comparative Medicine Program and Veterinary Resources,
10 South Pine Street, MSTF Room G-100, Baltimore, Maryland 212015.
History. A 23-year-old intact female rhesus macaque (Macaca
mulatta) weighing 8.4 kg was examined for a mass in the region of a
supranummary right teat located adjacent to and below the normal
right teat. Th is subcutaneous mass was 2.5 cm in diameter, fi rm,
lobulated, and moveable on palpation. Th is monkey was born in
1977 in a domestic colony; was used in a breeding colony from 1985
to 1993; was negative for B virus, produced seven live off spring; and
received no reported treatment with exogenous hormones. She was
transferred to the University of Maryland School of Medicine in
1996 and placed on an institutional animal care and use committee
(IACUC)-approved study of aging in macaques. Th e presence of a
mass fi rst was noted on arrival, when it was 1.5 cm in diameter. It
was not considered a noteworthy fi nding initially. When enlargement
was noted during examination for an unrelated problem in 1999,
further diagnostic evaluation was undertaken. Diff erential diagnoses
for this mass included mammary or sebaceous gland hyperplasia,
and neoplasia (adenoma, carcinoma in situ, lobular carcinoma,
ductal carcinoma, lipoma, or granulomatous tissue). Th is animal
had been singly housed, with visual and auditory interaction with
other monkeys, per approved protocol justifi cation, in an Association
for the Assessment and Accreditation of Laboratory Animal Care,
International-accredited facility since 1996, was fed a commercial
primate diet, and received environmental enrichment treats including
fruit, cereals, and fresh vegetables and other enrichment devices per
an IACUC-approved primate enrichment plan.
In November 1999, the macaque was presented for veterinary
evaluation of mildly decreased appetite and soft-tissue swelling of
A 23-year-old female rhesus macaque presented with a 2.5-cm diameter, fi rm, moveable, lobulated subcutaneous mass associated with
a supranummary teat on the right side of the chest. Th is animal was a retired breeder, currently in an aging study. No exogenous hor-
mone treatments were noted in the animal’s history. Chest radiographs were within normal limits. Blood screens showed no noteworthy
variations from normal. Needle aspirate cytology showed clusters of neoplastic cells. Grossly the mass was well circumscribed, fi rm, and
homogeneously tan, with a glandular appearance. Diff erential diagnoses included sebaceous or mammary adenoma, carcinoma in situ,
and lobular or ductular carcinoma. Histopathology was consistent with a mammary ductal carcinoma with comedo pattern. Subsequent
needle aspirate cytology from an adjacent right axillary lymph node showed tumor cells with a few lymphoid cells, interpreted as lym-
phatic spread. Chest radiographs 2 and 6 weeks postbiopsy showed no evidence of pulmonary metastasis. After 1 year, there was no
marked change on chest radiographs, but a small cluster of new nodules was palpable in the right axillary region. Histopathology of an
excisional biopsy of the new nodules indicated tumor growth subjacent to regional lymph nodes. Further treatment was not performed
and the animal remained clinically normal fi ve years after the initial diagnosis. Spontaneous mammary neoplasia is a major concern in
human medicine, yet it rarely has been reported to occur in nonhuman primates. Th is case is important in documenting an additional
case of spontaneous mammary tumor development.
the left shoulder joint. An acute soft tissue injury was diagnosed and
responded well to analgesic therapy. However, during the physical
examination, enlargement of the reported mass was noted, and a
decision was made for diagnostic evaluation because of increasing
size of the mass.
A fi ne-needle aspirate showed multiple irregular clusters of large,
basophilic, pleomorphic epithelial cells with no distinct architecture,
demonstrating a high nuclear-to-cytoplasmic ratio, enlarged nucleoli,
and numerous mitotic fi gures, thus meeting criteria for neoplasia. Th e
neoplastic cells were surrounded by a background of infl ammatory
cells including neutrophils, lymphocytes, and macrophages (Fig. 1).
Complete blood count with diff erential and standard serum biochem-
istry (electrolytes, glucose, blood urea nitrogen, creatinine, calcium,
phosphorus, serum protein, albumin, globulin, creatinine phospho-
Figure 1. Cytology of fi ne needle aspirate. Presurgical cytologic preparation
showing multiple clusters of large, round, dark blue staining pleomorphic
cells with high nuclear to cytoplasmic ratio, surrounded by subacute infl am-
matory cells including neutrophils, lymphocytes, and monocytes. Clusters
interpreted as neoplastic cells. Diff Quick stain.
Volume 44, No. 4 / July 2005 CONTEMPORARY TOPICS © 2005 by the American Association for Laboratory Animal Science
kinase, aspartate aminotransferase, alanine aminotransferase, alkaline
phosphatase, lactic dehydrogenase, gamma glutamyltransferase,
direct and indirect bilirubin, triglycerides, cholesterol, magnesium,
iron, amylase, and lipase) essentially were normal. Chest radiographs
showed normal aging changes with no radiographic evidence of
In light of the cytology and favorable results of preliminary hema-
tologic, serologic, and radiologic screening, wide surgical excisional
biopsy was performed according to standard veterinary surgical pro-
cedures. Th ese included use of aseptic surgical technique, isofl urane
anesthesia after induction with ketamine, continuous evaluation of
vital signs and anesthetic depth by a trained veterinary technician
using visual and mechanical monitoring techniques, intravenous
fl uid support, analgesics, and antibiotics. Th e tumor was well cir-
cumscribed, with no visible extensions beyond the local borders.
It was fi rm with a homogeneous consistency, tan on cut surface,
and surrounded by fat and overlying skin. Th e tumor was placed in
10% neutral buff ered formalin and submitted for histopathology.
Recovery of the animal was routine. Postoperative treatment included
buprenorphine at 0.03 mg/kg twice daily for 2 days and enrofl oxacin
at 5 mg/kg once daily for 5 days.
One week after surgery, the animal opened a portion of the incision
and was sedated for examination and repeat closure of the incision. At
the time there was mild swelling in the right axillary region with a small
lump presumed to be an axillary lymph node. Needle aspirate from
this lump showed cells similar to the presurgery cytology in a back-
ground of adipose tissue. Th ere were macrophages, neutrophils, and
lymphocytes consistent with chronic, but active, mild infl ammation.
Further treatments such as radical mastectomy, ovariohysterectomy,
chemotherapy, and hormone therapy were considered. Because of
a lack of historical treatment protocols for mammary neoplasia in
macaques and the desire not to add confounding variables that might
exclude the animal from the research protocol for the study of aging,
the attending veterinarian and investigator decided to monitor the
animal closely without further therapy. Th ere were no clinical signs
related to the tumor that indicated current pain or distress necessitat-
ing euthanasia. It was agreed that if decline in the animal’s well-being
became an issue, euthanasia would be performed.
Quarterly follow-up examinations of the animal included physical
examination, chest radiography, hematology, and serum chemistry
panels. At 1 year postsurgery, a small cluster of 2- to 5-mm focal
nodules were palpable in the right axillary region. Th ese were removed
surgically, and histopathology showed tumor growth associated with
lymph nodes and lymphatics, with appearance very similar to the
cytology shown in Fig. 1. Chest and abdominal radiographs did
not show visible metastases, and blood work remained essentially
normal. After fi ve years of follow up the monkey continued to do
well, with small localized, nodules but no clinical or radiographic
signs of metastatic disease.
Histology procedures. Paraffi n-embedded samples of mammary
gland were cut into 5-μm sections and stained with hematoxylin and
eosin (H&E), periodic acid–Schiff (PAS), PAS–diastase, and Alcian
blue (pH 2.5 and 1.0). For mucicarmine staining, a commercial kit
(Bio Optica, Milano, Italy) was used.
Immunohistochemical assays were done according to standard
methods by using a commercial streptavidin–biotin peroxidase
labeling kit (DAKO, Glostrup, Denmark) and diaminobenzidine as
chromogen (0.04% for 7 min). Endogenous peroxidase was blocked
by treatment with 3% hydrogen peroxide for 30 min. Th e sections
then were immersed in citrate buff er (2.1 g citric acid monohydrate
per liter of distilled water; pH 6.0), heated for four 5-min. periods
in a microwave oven at 750 W, and cooled at room temperature for
20 min. Th e primary antibodies (DAKO) consisted of monoclonal
antibodies against cytokeratin 19 (clone BA 17, diluted 1:40), smooth
muscle alpha-actin (clone 1A4, diluted 1:100), vimentin (clone V9,
diluted 1:40), and Mac 387 (monoclonal mouse anti-human my-
eloid/histiocyte antigen, clone Mac 387; 1:100). All antibodies were
incubated overnight at 4°C. Th e reaction was developed by using
peroxidase (Labeled Streptavidin biotin System-LSAB, DAKO). Th e
chromogen diaminobenzidine (0.04%, 7 min at room temperature)
was used, and then the sections were counterstained with Papanicolau
hematoxylin, rinsed in tap water, dehydrated, and mounted with
DPX Mountant (distrene, plasticizer, xylene, Fluka Chemie AG,
Buchs, Switzerland). Pathology procedures were performed at the
University of Bologna (Italy).
Pathology. Grossly the tumor appeared as a fi rm, tan, lobulated,
subcutaneous mass, without a distinct capsule. Th ere was no gross
evidence of invasion into the subjacent musculature. At low magni-
fi cation, the tumor showed multilayered to solid carcinomatous areas
intermingled with an intense desmoplastic stroma. Th e carcinoma
appeared as distended ductal structures lined by a multilayered epi-
thelium, often lacking lumina, and with surrounding necrotic debris
in a comedo pattern. At higher magnifi cation, the neoplastic cells
showed indistinct cell borders, scant slightly eosinophilic cytoplasm, a
prominent nucleus with clumped chromatin, and a single nucleolus.
Mitotic fi gures were frequent. Among the neoplastic cells there were a
number of globoid cells, with distinct cell boundaries, cytoplasm from
uniformly eosinophilic to fi nely vacuolated, often with an eccentric
nucleus (“signet ring” cells). Th ese larger cells were frequently inter-
mingled with the carcinomatous counterpart and sometimes formed
small clusters (Fig. 2A and B). Both cell types stained positively for
cytokeratin 19 and negatively for vimentin and Mac 387. (Fig. 3 and
4). Histochemical stains did not reveal any mucicarmine, PAS, Alcian
blue pH 2.5-and 1.0-positive content in either cell type (Fig. 5). Th e
desmoplastic stroma surrounding the carcinoma was infi ltrated with
infl ammatory cells, mostly lymphocytes and eosinophils.
Pathology discussion. Th e presence of large multilayered to solid
areas suggests a ductal origin of the tumor. Th e cells forming the neo-
plastic mass have the features of a comedo carcinoma of ductal origin,
with accumulation of cell detritus and necrosis in the lumina. Th e epi-
thelial origin of the cells is demonstrated by the immunohistochemical
positive reaction to anti-cytokeratin 19 and the negative reaction to
vimentin. Th e only cells that stained positive for alpha-actin, which
were those of the smooth muscle admixed with the connective tissue
forming the adjacent stroma and the vascular walls.
Th e numerous globoid cells observed among the typical epithelial
neoplastic cells (which resembled morphologically those of a muci-
nous carcinoma were confi rmed to be of epithelial origin (cytokeratin
19 positive) but do not produce mucinous substance. In fact, although
their morphology resembles signet ring cells in mucinous carcinoma
their content stains negative for mucicarmine, PAS, and Alcian blue
(pH 2.5 and 1.0), which are all methods to reveal mucin. Th e PAS
negativity also indicates low glycogen content, allowing for the
exclusion of the so-called glycogen-rich carcinoma of human breast
cancer. Th e vacuolated appearance of most cells is suggestive of a
lipid content (not demonstrable in our formalin-fi xed and paraffi n
embedded material) as in the so-called lipid-rich carcinoma known
in human breast as well as animal mammary gland tumors.
Th e possible infl ammatory nature of these globoid cells as foamy
macrophages is excluded by the immunohistochemical negative stain
with the antibody Mac 387. As alpha-actin did not stain these globoid
cells, their nature as myoepithelial cells can also be excluded.
Spontaneous mammary neoplasia in nonhuman primates has
been described infrequently, and there is little to no information on
CONTEMPORARY TOPICS © 2005 by the American Association for Laboratory Animal Science Volume 44, No. 4 / July 2005
treatment beyond surgical excision. Few cases of primary mammary
neoplasia or neoplasia in supranummary mammary glands have been
described in the rhesus macaque, or other species of nonhuman pri-
mates. Th e majority of reports involving rhesus monkeys addressed
carcinomas, while other masses were described as nodular hyperplasia
(1-3, 5-8, 10, 11, 15-17). Four cases of spontaneous neoplasia in
rhesus macaques including ductal neoplasia similar to this case have
been reported (7, 8, 10, 17).
Teleki and Ford reported a spontaneous intraductal mammary
carcinoma in an adult female rhesus macaque with presentation very
similar to the present case. Th is animal was also treated by surgical
excision of the initial and subsequently developing nodules without
other therapy and remained clinically healthy for at least 2 years
from the initial surgery (17). Eydelloth and Swindle reported a case
of concurrent intraductal mammary carcinoma and benign ovarian
teratoma in an adult female rhesus macaque, but this animal had
received exogenous hormones as part of a reproductive study and died
due to trauma from a harem cagemate (8). Cohen, Saidla, and Schlafer
recently reported a spontaneous mammary gland ductal carcinoma in
situ in a 6- to 8-year-old multiparous female rhesus macaque, which
also was treated surgically (7). Spontaneous mammary carcinoma
with widespread metastases in a 22-year-old rhesus was reported by
Hubbard and colleagues as similar in behavior to infi ltrating duct
carcinoma, the most common breast cancer in women. Th is animal
survived for 5 years after detection of the initial tumor, having been
observed with no treatment reported (10). Two control rhesus in a
contraceptive study developed multiple small mammary nodules,
which were diagnosed as mammary nodular hyperplasia (15). Th ese
excised nodules diff ered from the current tumor, having fewer layers
of cells and more distinct acinar borders. Several possible etiologic
explanations for macaque mammary neoplasia have been postulated,
including the Mason–Pfi zer monkey virus described by Chopra and
others to occur in nonhuman primate mammary tumors (5, 6). Th is
virus has been found in mammary tissue of animals which do not
develop neoplasia as well and is not considered a primary etiologic
factor (7). Cohen and colleagues postulate that androgens, growth
hormones, irradiation, and aging may all have tumorigenic infl uence
on the mammary gland (7).
For the purpose of the present report, we are not including those
cases in which the animals had received exogenous hormone treatment
as part of a research protocol. However, one such report noted the
rarity of breast cancer in monkeys not receiving hormone therapy as
support for their case having a hormonal cause (11). Another noted
that the occurrence of spontaneous tumors in control animals needed
to be considered in the evaluation of mammary tissue in toxicologic
studies of contraceptives and other drugs (15).
From a review of the literature, spontaneous mammary neoplasia
appears to be rare, or rarely reported, in nonhuman primates. Multiple
reports on the same tumor cases and disagreement among pathologists,
both veterinary and human, on the naming of mammary tumors make
quantifi cation diffi cult, but the number of spontaneous mammary
neoplastic lesions reported to have occurred in rhesus macaques is
approximately 12. Th e infrequent occurrence of spontaneous mam-
mary neoplasms in macaques may be due to the limited numbers of
middle-aged to geriatric nonhuman primates available for study, to lack
of reporting, or to true low incidence. In Beniashvili’s 1988 overview
article, he suggested that the relative youth of monkeys usually kept
in primate facilities might be a reason for the infrequent reports of
spontaneous neoplasia, and he also noted a general increase in neoplasia
in monkeys older than 10 years when compared with younger animals
(2). Again in 2001, Cohen and coworkers commented on the rare
reporting of spontaneous mammary gland tumors in rhesus monkeys,
postulating that this paucity might refl ect species resistance or a lack
of thorough routine necropsy or examination (7).
Figure 2. Surgical biopsy of ductal carcinoma with comedo pattern. (A) Multilayered to solid carcinomatous areas intermingled with intense desmoplastic
stroma. Note distended ductal structures lined by a multilayered epithelium, either surrounding necrotic debris in a comedo pattern or with absent lumina.
H&E; magnifi cation, ×4. (B) Th e ductal carcinoma appears formed by two cell types, one characterized by large globoid cells fi lled with abundant granular
faintly eosinophilic cytoplasm, with an eccentric nucleus (signet ring cell, thin arrow) the other showing indistinct cell borders, a prominent nucleus and a
single nucleolus (large arrow). H&E; magnifi cation, ×20.
Figure 3. Immunohistochemical stain by anti-vimentin antibody showing
negative carcinomatous fi elds (arrow) and positive stromal septa. Magni-
fi cation, ×5.
Volume 44, No. 4 / July 2005CONTEMPORARY TOPICS © 2005 by the American Association for Laboratory Animal Science
In the presented case, the attending veterinarian and investiga-
tor elected to use surgical excision of the mass alone, with diligent
monitoring postsurgery. Th is decision was made due to the age of
the animal, lack of well-defi ned protocols for medical management
of breast associated tumors for this (or other veterinary) species, and
a desire not to add confounding variables to the research protocol.
We did not identify defi nitive factors that would indicate the need
for additional therapy based on discussions of human (primate)
mammary neoplasia. It was agreed that if metastatic spread to lungs
or other tissues occurred and compromised the health of the animal,
euthanasia would be performed. As of October 2004, at 28 years of
age, the monkey remained clinically unaff ected. Th is case demon-
strates a spontaneous, locally invasive, mammary ductal carcinoma
in a rhesus macaque, with minimal (if any) clinical eff ects on the
well being of the animal.
Surgical excision with wide margins is the primary treatment for
mammary neoplasia in the veterinary literature. Although ovario-
hysterectomy in dogs at an early age (before the fourth estrus) has
been shown to decrease incidence of mammary neoplasia, it has
not been shown to alter prognosis after neoplasia develops (4). One
study reported the use of tamoxifen (0.42 mg/kg orally twice daily)
as eff ective for treating dogs with mammary adenocarcinoma (12).
Eff ective was defi ned as objective tumor response in fi ve of seven
dogs with inoperable or metastatic tumor. However, mean survival
time was reported to be 4 months. Tamoxifen frequently causes
estrogen-like side eff ects such as vulvar swelling, vaginal discharge,
urinary tract infections, and incontinence (4, 13, 17). Th ere have also
been reports in the veterinary literature of the use of doxorubricin
and cyclophosphamide (9), but no consensus has been reached on
the effi cacy of this approach. In cats, side eff ects of this treatment
include severe anorexia and mild myelosuppressive eff ects (4). Th e
veterinary literature does not provide clear or convincing consensus
on the use of adjunctive chemotherapy or hormonal therapy in the
treatment of mammary neoplasia. Th e likelihood of noteworthy side
eff ects that would reduce quality of life and the uncertain benefi t of
this tumor also guided a decision not to pursue these options in this
case. Th e decision seems to have been borne out by the signifi cant
interval free of clinical disease for this animal.
Th e current case report is submitted in hopes that increased re-
porting of spontaneous tumors in these animals may lead to a better
understanding of the diff erences and similarities among primate spe-
cies and contribute to our understanding of comparative mammary
disease in animals and humans. Laboratory animal veterinarians,
toxicologists, and research scientists need to have information on the
incidence of spontaneous lesions in the animals they study in order to
interpret the signifi cance of lesions seen in clinical study situations.
Th is was succinctly stated by Lowenstine (“Th ere is no such thing
as a generic monkey!”) in her discussion of lesions and nonlesions
in primate pathology (14). Although our case does not present an
unreported tumor type, it adds additional data to the epidemiologic
record and may serve to stimulate further clarifi cation of the true
incidence of such tumors in rhesus monkeys, macaques in general,
and other species of nonhuman primates.
We thank Katherine Bullock, Robert Wesley, and Th eresa Alexander for
excellent clinical assistance with this case; Sara Kripowicz for processing tis-
sues; and Steven Shipley, DVM for extensive review of the manuscript.
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Figure 4. Immunohistochemical stain by anti-CK19 antibody, showing strong
positivity in the peripheral condensed rim of the cytoplasm in the globoid cells
(arrow) and faint focal positivity in the cytoplasm of ductal carcinomatous
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Figure 5. PAS negativity of the globoid cells (arrows) exclude a mucinous
content. Magnifi cation, ×20.
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