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Home , Breast cancer, Comedocarcinoma

pISSN 1598-298X J Vet Clin 30(6) : 486-489 (2013)

Mammary in a Dog Jae-Hoon Kim* and Jae-Hoon Kim1

College of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University, Jeju 690-756, Korea *Gyeonggi-do Livestock and Veterinary Service, Suwon 441-460, Korea

(Accepted: December 09, 2013)

Abstract : An 18-year-old, neutered female, Yorkshire terrier was presented with abdominal mass. Large abdominal mass was located in right 4th and 5th mammary . Surgically excised mammary mass was submitted for histological evaluation. Microscopically, multifocal to confluent neoplastic foci were existed from superficial dermis to subcutis. Several different growth patterns such as comedo, solid, cribriform, and micropapillary were present in the neoplastic foci. Large neoplastic mammary ducts showed great invasive tendency to adjacent tissues. Many superficial lymphatic plexuses and dermal lymphatics contained numerous neoplastic cell emboli. Because comedo pattern was demonstrated by more than 50% of the neoplastic cell population, we confirmed this case as mammary comedocarcinoma according to recent classification of canine mammary tumors. Key words : comedocarcinoma, dog, mammary mass, neoplastic cell emboli.

Introduction have been reported in Korean human medicine (8). In this study, we describe a case of invasive mammary ductal Canine mammary tumors (MGTs) are one of the in an old dog. To the author’s knowledge, this is most common in the bitch (11). The prevalence of the first case of canine mammary comedocarcinoma based on MGTs varies remarkably in different countries. The ratio of the most recent classification of canine MGTs in Korea. malignant to benign mammary tumors in dogs in most stud- ies is 3:7 or 4:6 (10). Among the benign tumors, complex Case and benign are the most common in dogs (10,11). Simple and complex are recorded An 18-year-old, neutered female, Yorkshire terrier was pre- as the most common type of malignant canine MGTs (10,11). sented for evaluation of a mammary mass. The abdominal Mammary carcinomas are quite heterogeneous in terms of mass was located between the right 4th and 5th mammary morphology and biological behaviors, and have been the glands (Fig 1). Three years ago, this dog received ovariohys- focus of several researches over the last few decades (11). terectomy due to pyometra. Physical examination, complete Two histologic classification systems for canine mammary blood count (CBC), serum chemistry profile, radiography, tumors and dysplasia have been proposed: the first in 1974 and ultrasonography were performed. Results of blood works and a modification in 1999 (10,11). However, since the pub- lication of the second system, several new histology sub- types of canine mammary neoplasms have been described (6). The authors proposed new histologic classification and nomenclature of neoplasms and dysplasia of the canine mam- mary gland. Some neoplasms that are incorporated into new classification system are included as specific entities. These include the cribriform type of simple carcinoma and come- docarcinoma, both of which were described under carci- noma-in situ (10). Several surveys of MGTs in dogs were previously reported in Korea (3,9,13). However the classification of MGTs in most surveys was performed based on the second classifica- tion of MGTs in 1999. Many ductal carcinomas arising from

1Corresponding author. Fig 1. Large abdominal mass (black circle) was located in right E-mail : [email protected] 4th and 5th mammary glands of dog. 486 Mammary Comedocarcinoma in a Dog 487

Fig 4. Large neoplastic mammary ducts showed invasive tendency Fig 2. Multifocal to confluent neoplastic foci were existed from (arrows) to adjacent connective tissues and lymphatic. H&E, superficial dermis to subcutis. H&E, × 100. × 200.

Fig 3. Comedocarcinoma in canine . Note central Fig 5. Note emboli of neoplastic cells in superficial lymphatic (N) in dilated mammary ducts. H&E, × 200. plexus. H&E, × 200. were within reference ranges. Abnormalities in serum chem- istry profile included increased in BUN (33.0 mg/dl; refer- patterns such as comedo, solid, cribriform, and micropapil- ence range, 8 to 25 mg/dl), increased ALP activity (189 U/L; lary were presented in the neoplastic mammary mass. Some reference range, 20-150), and GGT activity (19 U/L; refer- mammary ducts showed moderate to severe multifocal atypi- ence range, 1-15). Abdominal radiography and ultrasonogra- cal proliferation of ductal columnar . Most neo- phy revealed cardiac hypertrophy and hepatomegaly without plastic mammary ducts showed marked expansion and filled pulmonary abnormality. For histological evaluation the mass with sheets of ductal epithelial cells. These neoplastic cells was surgically removed. The mass was fixed in 10% buff- had round to oval nuclei with prominent nucleoli, scant baso- ered formalin and submitted to the laboratory of philic cytoplasm and high mitosis (5 or 6 per high power College of Veterinary Medicine in Jeju National University. field). Because of heavy proliferation of ductal epithelial cells Submitted mammary mass was trimmed, embedded in par- with multiple layers, many mammary ducts showed severe affin, sectioned at 3 µm, and stained with hematoxylin and dilatation and usually had central caseous necrotic area eosin (H&E) for light microscopic examination. (comedo carcinoma, Fig 3). These neoplastic ducts were sur- Histopathologically, covered epidermal was relatively nor- rounded by dense connective tissue with the infiltration of mal. Multifocal to confluent neoplastic foci were existed from chronic inflammatory cells. Large neoplastic mammary ducts superficial dermis to subcutis and were not circumscribed showed invasive tendency to adjacent connective tissues (Fig with dense connective tissue (Fig 2). Several different growth 4), therefore small daughter nests of were formed 488 Jae-Hoon Kim and Jae-Hoon Kim around primary sites. Cribriform pattern characterized by the comedo DCIS is the type of DCIS most commonly associ- forming a sievelike arrangement of neoplastic epithelial cells ated with microinvasion in human medicine (7). Similar his- and micropapillary pattern were also presented adjacent of topathologic findings also demonstrated in canine MGTS. large neoplastic foci. Many superficial lymphatic plexuses and According to one retrospective study on canine mammary other dermal lymphatics contained numerous neoplastic cell carcinomas, the occurrences of the infiltrative growth and the emboli (Fig 5). However relatively normal mammary glands lymphatic vessels of tumor cells was more preva- were scattered in or around neoplastic foci. Because comedo lent in comedocarcinoma than other carcinomas such as sim- pattern was occupied more than 50% of the neoplastic cell ple tubular, simple solid, complex carcinoma and ductal population, we confirmed this case as comedocarcinoma. carcinoma (14). Major comedo pattern and other minor pat- Two histological systems have been used for canine terns such as cribiriform and solid form were coexistent in and feline mammary carcinomas (11,14). Several parameters the report. However, very strong invasion of tumor cells and such as tubule formation, nuclear pleomorphism, mitotic lymphatic emboli were noted in the structures of comedocar- activity, and anaplasia were included in these grading sys- cinoma. tems. The sum of individual scores determined the histologi- In the pre- era, the diagnosis of human cal grade of . Based on the grading system, DCIS was uncommon (7). It was accounted for only 1-2% of comedocarcinoma in this case was determined as grade III newly diagnosed breast , and usually detected when it tumor. formed a large palpable mass (1). was regarded as a standard therapy at this time. In some instances, how- Discussion ever, DCIS can recur locally, and 50% recur as invasive car- cinoma (7). Considering the development of mammography Mammary is the most common type of for the detection of breast cancers during past two decades, breast in women (1,15), including invasive (or infil- recent DCIS accounts for 20-30% of all diagnosed breast can- trating) ductal carcinoma (IDC) and cer. This detection method also has great benefits such as easy (DCIS) (15). IDC is the most common type of invasive to access and early detection of DCIS. Therefore more effec- , accounting for 65% to 80% of invasive breast tive therapies including , post-operative , lesions (16). DCIS is a proliferation of epithelial cells origi- and adjuvant endocrine therapy have been adopted for human nating within the terminal -lobular unit (TDLU) of the DCIS. According to previous literatures, many evidences breast and limited by the surrounding basement membrane supported the hypothesis that canine DCIS are the intermedi- (7). The proliferation can usually be subdivided morphologi- ate precursors of invasive malignant tumor in canine mam- cally into ductal and lobular types based on architecture and mary glands (2,4,12). More accurate detection methods for cytology, rather than the origin of the cells, since both types canine MGTS, especially in DCIS, and effective therapeutic are presumed to arise from TDLU. The types of human protocols should be warranted in veterinary medicine. DCIS were classified primarily on their predominant micro- scopic growth pattern, which included comedo, cribriform, References solid, papillary, micropapillary, and clinging (1,7). In recent veterinary literatures, new or additional morphologic sub- 1. Allred DC. Ductal carcinoma in situ: terminology, classifi- types of canine MGTs with specific histologic and clinical cation, and natural history. J Natl Cancer Inst Monogr 2010; features have been described, hence some neoplasms such as 41: 134-138. cribriform type of simple carcinoma, comedocarcinoma, duc- 2. Antuofermo E, Miller MA, Pirino S, Xie J, Badve S, tal carcinoma, and micropapillary carcinoma have been Mohammed SI. Spontaneous mammary intraepithelial lesions in dogs--a model of breast cancer. Cancer Epidemiol Bio- incorporated into the new WHO classification (5,6,14). In markers Prev 2007; 16: 2247-2256. this case, extensive stromal invasion and vascular invasion in 3. Chae HC, Byeon YE, Lee ST, Lim JH, Kweon OK, Kim numerous lymphatics were observed throughout the mam- WH. Mammary gland tumors treated by surgical excision: a mary mass. In addition, multi-lobulated neoplasm with huge retrospective study in 79 dogs. J Vet Clin 2007; 24: 331-336. and well-demarcated central necrosis was occupied more than 4. Ferreira E, Gobbi H, Saraiva BS, Cassali GD. Histological 50% of the neoplastic cell population as previously described and immunohistochemical identification of atypical ductal (14). Therefore we confirmed this case as comedocarcinoma mammary as a preneoplastic marker in dogs. Vet according to recent classification of canine mammary tumors (6). Pathol 2012; 49: 322-329. Comedo DCIS in human tends to be larger than other 5. Gama A, Alves A, Schmitt FC. Clinicopathologic features of forms of DCIS. The name “comedo” in this type was coined mammary invasive micropapillary carcinoma (IMC) in dogs. from its gross appearance, because the necrotic cellular Vet Pathol 2008; 45: 600-601. 6. Goldschmidt M, Peña L, Rasotto R, Zappulli V. Classification debris oozed from the ducts when the excised tumor was and grading of canine mammary tumors. Vet Pathol 2011; squeezed, resembling comedones (1). A large proportion of 48: 117-131. human DCIS up to 50% showed complex combinations of 7. Jaffer S, Bleiweiss IJ. Histologic classification of ductal growth patterns and cellular features (1,15). Widespread carcinoma in situ. Microsc Res Tech 2002; 59: 92-101. Mammary Comedocarcinoma in a Dog 489

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개에서 발생한 유선 면포암종

김재훈*·김재훈1 제주대학교 수의과대학, 수의과학연구소, *경기도 축산위생연구소

요약:18세령 중성화 암컷 요크셔테리어종 개가 우측 4번 및 5번 유선 부위에 위치한 대형 복부 종괴로 내원하였 다. 외과적으로 적출한 유선 종괴가 병리학적 진단을 위하여 의뢰되었다. 병리조직학적 소견으로 종괴는 표피에서 피 하조직에 걸쳐 다발성 및 융합된 종양성 집락들로 구성되어 있었다. 종양성 집락들은 면포상, 고형상, 사상 및 미세유 두상 등의 매우 다양한 형태를 나타내었으며, 큰 종양성 유선 도관은 주변조직으로의 강한 침습성을 나타내고 있었다. 진피표층에 위치한 다수의 림프관 얼기들과 진피의 림프관에는 무수히 많은 종양세포의 색전을 가지고 있었다. 종양 을 구성하고 있는 세포들의 약 50%이상이 면포상의 형태를 띠고 있기 때문에, 본 증례는 최근의 개 유선 종양의 분 류에 근거하여 개의 유선에서 발생한 유선 면포 암종으로 진단하였다. 주요어 : 개, 면포암종, 유선 종괴, 종양세포 색전.