ACTA

AMAZONICA http://dx.doi.org/10.1590/1809-4392202300201

ANIMAL AND FISHERIES SCIENCES | SHORT COMMUNICATION

Anaplastic mammary carcinoma in a captive jaguar

(Panthera onca)
Camila TOCHETTO1, Guilherme Augusto MARIETTO GONÇALVES2, Diogo Souza ZANONI3,
Renato Lemos PEREIRA4, Gisele Torres Clímaco de ARAÚJO5, Renan Mori ROCHA5,
Bruna Carolina ULSENHEIMER6, Alexandre Alberto TONIN7*
1
Exército Brasileiro, 13ª Companhia Depósito de Armamento e Munição (Cia DAM), Itaara, Rio Grande do Sul, Brazil
2
Doc.Bird Consultoria em Medicina Aviária, Animais Exóticos e Silvestres, Botucatu, São Paulo, Brazil
3
Universidade Estadual Paulista (UNESP), Faculdade de Medicina Veterinária e Zootecnia (FMZV), Botucatu, São Paulo, Brazil
4
Exército Brasileiro – Academia Militar das Agulhas Negras (AMAN), Rezende, Rio de Janeiro, BrazilAA-2023-0020
5
Exército Brasileiro, Centro de Instrução de Guerra na Selva/Zoológico (CIGS), Manaus, Amazonas, Brazil
6
Universidade Federal de Santa Maria (UFSM), Programa de Pós-graduação em Medicina Veterinária, Santa Maria, Rio Grande do Sul, Brazil
7
Instituto Federal de Educação, Ciência e Tecnologia do Amazonas (IFAM) - Campus Manaus Zona Leste, Manaus, Amazonas, Brazil
* Corresponding author: alexandre.tonin@ifam.edu.br; https://orcid.org/0000-0002-4236-8976

ABSTRACT
A captive female of jaguar (Panthera onca), 12 years old, presenting an 8-day history of anorexia and lethargy, died in its enclosure
in Manaus (Amazonas, Brazil). The necropsy revealed an abdominal multinodular ventral plaque into the mammary region.
Additionally, in several locations of the subcutaneous tissue, there were multiple metastatic nodules of firm texture. Metastases
were also observed in the lymph nodes, heart and lungs. The immunohistochemistry results revealed the cytoplasmic staining
for cytokeratin on neoplastic cells, mild staining (+) for E-cadherin, moderate staining (++) for estrogen and progesterone
receptors, and about 50 to 70% of staining for Ki-67. The neoplastic cells were negative for vimentin staining. Therefore, the
histopathological examination led to a diagnosis of metastatic anaplastic mammary carcinoma, which is an unusual condition
in wild felines.
KEYWORDS: Amazon, Felidae, neoplastic disease, wild feline

Carcinoma mamário anaplásico em uma onça-pintada (Panthera onca)

criada em cativeiro
RESUMO
Uma onça pintada (Pantera onca) de cativeiro, fêmea, de 12 anos, com história clínica de 8 dias de anorexia e letargia, foi
encontrada morta em seu recinto em Manaus (Amazonas, Brasil). Na necropsia foi observada uma placa abdominal ventral
multinodular na região mamária. Em várias regiões do tecido subcutâneo, foram observados diversos nódulos metastáticos
de consistência firme. Metástases também foram observadas nos gânglios linfáticos, coração e pulmões. Os resultados da
imuno-histoquímica (IHQ) revelaram coloração citoplasmática para citoqueratina nas células tumorais, coloração leve (+)
para E-caderina, moderada (++) para receptores de estrogênio e progesterona e cerca de 50 a 70% de coloração para Ki-67.
As células neoplásicas foram negativas na IHQ para vimentina. Assim, o exame histopatológico conduziu a um diagnóstico
de carcinoma mamário anaplásico metastático, que é uma condição incomum em felinos selvagens.
PALAVRAS-CHAVE: Amazônia, Felidae, doença neoplásica, felino selvagem

CITE AS: Tochetto, C.; Marietto Gonçalves, G.A.; Zanoni, D.S.; Pereira, R.L.; Araújo, G.T.C.; Rocha, R.M.; Ulsenheimer, B.C.; Tonin, A.A. 2023. Anaplastic
mammary carcinoma in a captive jaguar (Panthera onca). Acta Amazonica 53: 281-284.

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AMAZONICA Tochetto et al. Anaplastic mammary carcinoma in a jaguar

In nondomestic felids, mammary neoplasms, usually multiple nodules, white to reddish (Figure 1c), with firm
of malignant development, have been reported with higher texture, and varying from 0.3 to 2.0 cm in diameter (Figure
incidence in tigers, Panthera tigris L., than in other captive 1b). The parenchyma of the superficial axillary and inguinal
felids like jaguar, Panthera onca L., lion, Panthera leo L., lymph nodes was replaced by a firm and white tissue. In the
leopard, Panthera pardus L., puma, Puma concolor (Linnaeus, myocardium, there were multiple nodules, small, firm and
1771), and jungle cat, Felis chaus Schreber, 1777 (Harrenstien whitish with not more than 0.3 cm in diameter. Likewise,
et al. 1996; Munson and Moresco 2007; Sadler et al. 2016). there were some well delimited nodules in the lungs, firm,
Most of the mammary tumors observed in felids kept in whitish and measuring no more than 1.5 cm in diameter. From
zoos had an aggressive pattern, often invasive and metastatic, the lungs, after incision, flowed a large amount of liquid and
similarly to when diagnosed in domestic cats, Felis catus L. there was a white foam throughout the length of the trachea,
(Finotello et al. 2011; Munson and Moresco 2007; Sadler indicating a possible pulmonary edema.
et al. 2016). Here we describe the gross histological and The samples were fixed by immersion in buffered
immunohistochemical features of an anaplastic mammary 10% formalin for later microscopic evaluation. The
carcinoma in a captive jaguar, a condition which so far had histopathological examination revealed that the tumor
not been reported in P. onca. tissue was composed of exceedingly invasive and scattered
A captive female jaguar, about 12 years old, from Manaus, individualized or small grouped neoplastic cells, with a
Amazonas state, Brazil), died in its enclosure (in a private hotel round, oval, or polygonal shape, showing mild to moderate
mini zoo) after an 8-day history of anorexia and lethargy. The anisocytosis (Figure 2a). Some of the neoplastic cells had lost
necropsy revealed a multinodular plaque into the mammary the junctional properties, as typically observed in cells of
region (inguinal to abdominal direction), measuring 12.0 x epithelial origin. The nuclei of neoplastic cells are generally
8.0 x 1.0 cm. The skin over this specific region had areas of huge and round or oval. However, in this case, they are highly
ulceration. Through a surface cut, it was observed that the mass pleomorphic and exhibit moderate anisocariosis, multiple
was extending from the superficial dermis to the subcutaneous nucleoli and several multinucleated cells. In addition, many
tissue (Figure 1a). Another mass was observed adjacent to mitotic figures were seen (mitotic index: 10 mitotic figures/10
the plaque measuring 6.0 x 2.5 x 1.5 cm, being solid/firm high-power fields/2.37 mm2). Moderate desmoplasia was
on surface cut and diffusely white. Into the subcutaneous observed around the neoplastic cells. Peritumoral neoplastic
tissue, in several regions of the animal body, there were emboli were observed within lymph vascular vessels, with
mild to moderate inflammatory infiltrations. Histological
analysis revealed the presence of some large pleomorphic
epithelial cells, grouped in small clusters with eventual
presence of bizarre nuclei. Our case was classified as grade
II based on tubule formation, nuclear pleomorphism and
mitotic count. Because neoplastic cells are very anaplastic,

Figure 1. A – Anaplastic mammary carcinoma (AMC) in a captive jaguar (Panthera

onca) from Manaus (Amazonas, Brazil), with neoplastic tissue extending from the Figure 2. A – Histopathology of the mammary gland tumor of a captive
superficial dermis to the subcutaneous tissue; B – Metastasis of the AMC with firm jaguar (Panthera onca) from Manaus (Amazonas, Brazil) showing tumor cells
nudules in the subcutaneous tissue (thoracic and abdominal lateral region); C – with infiltrative growth into the surrounding connective tissue (H.E); B –
Surface cut of the nodules in high magnification presenting white with reddish Immunohistochemical result showing neoplastic cells positive for cytokeratin.
areas. This figure is in color in the electronic version. Magnification 40x, scale bar = 50 μm. This figure is in color in the electronic version.

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immunohistochemistry was performed with cytokeratin Most cancers have some areas of tubulopapillary growth with
and vimentin (Sawa et al. 2017), E-cadherin (Furusawa et formation of solid, cribriform patterns and both intraductal
al. 2021), estrogen and progesterone receptors and Ki-67 and infiltrating components (McAloose et al. 2007). Our
antibodies (Dagher et al. 2019a). The immunohistochemistry case supports the literature, as we observed peritumoral
results revealed the cytoplasmic staining of cytokeratin in neoplastic emboli within lymphatic vascular vessels, with mild
neoplastic cells (Figure 2b), mild (+) staining for E-cadherin, to moderate inflammatory infiltrate.
moderate (++) staining for estrogen and progesterone receptors Histological grading is a good parameter to stratify tumors
and about 50 to 70% of staining for Ki-67. The neoplastic according to their biological aggressiveness. The Elston and
cells were negative for vimentin staining. Ellis (EE) histologic grading system, originally developed
Studies on tumors in wild felines are uncommon. A for human breast cancer, is commonly used to grade feline
review of medical records and necropsy reports in Knoxville mammary carcinomas (Dagher et al. 2019b) and has a strong
Zoological Gardens (USA) from 1979 to 2003 reported 40 correlation with prognosis, therefore was used in our case
neoplasic tumors in 26 felids (comprising the integumentary- report. Most diagnosed zoo felids had high-grade mammary
mammary, endocrine, reproductive, hematopoietic- cancer, mostly with metastatic disease at the time of diagnosis,
lymphoreticular, digestive, and hepatobiliary systems), regardless of their history of progestin exposure (Castagnaro
amounting to 28% of all death cases or reason for euthanasia et al. 1998; McAloose et al. 2007). Mammary carcinomas
of those felids (Owston et al. 2008). in domestic cats have comparable aggressive features, high
Failure of early detection of tumors in zoo felids is likely tumor grades (II or III), and evidence of metastasis at the
due to late diagnostic procedures, such as physical examination, time of diagnosis (Dagher et al. 2019b). These features
since animals are examined only opportunistically, and are associated with decreased survival in domestic cats, as
depend on scheduled anesthesia. In this context, early in human mammary cancer patients, and also are likely
clinical detection is difficult, as the absence of prominent important prognostic indicators in zoo felids (Castagnaro et
nodules prevents early clinical suspicion. However, there are al. 1998; McAloose et al. 2007).
indications that mammary cancer of high grade and metastatic Although feline mammary malignant tumors are frequent
potential develops early in the course of carcinogenesis in in non spayed female cats, anaplastic carcinomas have not
both domestic and zoo felids (McAloose et al. 2007; Munson yet been described in jaguars. The lack of information of
and Moresco 2007; Zappulli et al. 2015; Sadler et al. 2016). mammary tumors in P. onca may be due to a low prevalence
Mammary gland tumors have been associated with the of the disease in this species, associated with the difficulty in
use of the synthetic progestins melengestrol acetate (MGA) its clinical recognition and/or accurate diagnosis in wild or
(Harrenstien et al. 1996) and medroxyprogesterone acetate captive animals (McAloose et al. 2007). In contrast to other
(MPA) as a method of contraception (Black et al. 1979; types of mammary carcinomas, the anaplastic type in felids
Misdorp 1991) in both, domestic and zoo felids (McAloose is highly invasive and exhibits extensive amounts of collagen
at al. 2007). A correlation has been found between clinically fibres (scirrhous carcinoma), which is, in comparison, not
aggressive mammary carcinomas and MGA treatment in wild the typical presentation of anaplastic carcinomas in dogs and
captive felids (Black et al. 1979). However, in the present humans (Misdorp 2002).
case, there is no record of use of any contraceptive method. We confirmed that the cellular origin of the tumor in
Anaplastic mammary carcinoma is difficult to treat though our case was epithelial based on the immunohistochemical
surgery procedure, due to its early and extensive infiltration positivity for cytokeratin, and negative staining for vimentin
into the surrounding tissues and the lymphatic system (Kim (Kim et al. 2015). The low proportion of mammary cancer
et al. 2015), as observed in the present case. The regional positive for either progesterone (PR) or estrogen receptors
lymph nodes and lungs are the organs that are most frequently (ER) in zoo felids is similar to that reported for mammary
affected by metastases (Misdorp 2002). The most frequently carcinomas in domestic cats, which have fewer ER and PR
observed area of metastases in felines was the lungs (76.9%), receptors than in normal mammary gland or benign mammary
followed by the skin (23.1%) (Togni et al. 2013). Pleura, liver, tumors (Dagher et al. 2019a). PR status does not appear to
spleen, kidneys, bones, and brain may also be affected (Hayes correspond to prognosis in zoo felids, as both PR-positive and
et al. 1981). In our case, metastases were observed in skin, -negative cancers were of high grade with metastasis (De Las
inguinal and axillary lymph nodes, lung and heart. Mulas et al. 2000; McAloose et al. 2007).
The historical lack of consensus on morphological The strong expression of Ki-67 in our case, especially in
classification of domestic animal mammary tumors reflects the tumor cells, demonstrating mitotic figure, indicates that
controversies over histogenesis (Misdorp 2002). In domestic the tumor is highly malignant and aggressive. Similarly, most
and zoo cats, morphologic patterns of mammary cancer are reports on zoo felids stated a high-grade cancer with aggressive
like breast cancer in women (Munson and Moresco 2007). metastasis (McAloose et al. 2007; Yun et al. 2014).

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Anaplastic mammary carcinoma is uncommon in Hayes, H.M.; Milne, K.L.; Mandell, C.P. 1981. Epidemiological
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immunohistochemistry contributed for the diagnostic of an Kim, J.H.; Kim, W.J.; Park, J.; Shin, J.I.; Yoon, H.Y. 2015. Canine
mammary anaplastic carcinoma with concurrent aorto-iliac
anaplastic mammary carcinoma. No published reports on this
thrombosis in a dog: a case report. Veterinari Medicina 60:
type/classification of neoplasm existed so far for wild felines. 391-398.
McAloose, D.; Munson, L.; Naydan, D.K. 2007. Histologic features
ACKNOWLEDGMENTS of mammary carcinomas in zoo felids treated with melengestrol
The authors thank Nonato Aamaral and Daniel Henrique acetate (MGA) contraceptives. Veterinary Pathology, 44: 320-326.
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cats. Acta Endocrinologica, 12: 27-31.
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tumors of dogs and cats. Journal of Veterinary Medicine and RECEIVED: 26/01/2023
Science, 83: 1363-1368. ACCEPTED: 29/08/2023
Harrenstien, L.A.; Munson, L.; Seal, U.S. 2011. Mammary cancer ASSOCIATE EDITOR: Rodrigo R. do Valle
in captive wild felids and risk factors for its development: A DATA AVAILABILITY
mammary cancer in captive wild felids and risk factors for its The data that support the findings of this study are available, upon
development: a retrospective study of the clinical behavior of 31 reasonable request, from the corresponding author Alexandre Alberto
cases. Journal of Zoo Animal Medicine, 27: 468-476. Tonin.

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