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Laboratory of Veterinary Pathology, College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa, Japan
Abstract
The intra-abdominal tumor developing in the uterus and lung of a domestic Shorthair cat was examined histopathologically and immunohistochemically. The tumor showed a proliferation of both endometrial stromal and smooth muscle cells accompanied by prominent vasculature. There were well-differentiated endometrial glands, and tubuli made up a monolayer of eosinophilic cuboidal epithelium. Immunohistochemically, the spindle-shaped cells and half of the stromal-like cells reacted to caldesmon and desmin antibodies. The neoplastic epithelium expressed AE1/AE3 cytokeratin. Feline endometrial stromal tumor has, to the best of our knowledge, not been reported previously and has smooth muscle and glandular components that are a unique variant to the human counterpart.
Key words: Cat; endometrial stromal sarcoma; smooth muscle; uterus.
The majority of tumors developing in the feline uterus are adenocarcinomas. Although leiomyomas and leiomyosarcomas have sometimes been reported, malignant mesenchymal tumors, except lymphomas, occur rarely in the reproductive tract of cats.6 In women, endometrial stromal tumors are known to be rare tumors that have been characterized by the growth of tumor cells resembling nonneoplastic proliferative endometrium.1,4,8,12 Endometrial stromal sarcomas may show a variety of morphologic appearances, including epithelial differentiation, a sex cord-like pattern, smooth muscle differentiation, and fibrous/myxoid appearances. These variants often lead to the difficulties of a differential diagnosis among uterine mesenchymal tumors.10,11 This report describes a novel uterine neoplasm with components of endometrial stroma, smooth muscle, and endometrial glands that developed in the abdominal cavity of a queen and metastasized to the lungs.
A 12-year-old domestic Shorthair queen, weighing about 4.2 kg, was referred a local veterinarian with complaints of depression, anorexia, panting, vomiting, and a purulent vaginal discharge. The abdominal palpation revealed a 3 x 10 cm solid mass in the abdominal cavity. Thoracic radiographs showed that the different-sized masses measured less than 1.5 cm in diameter in the lungs. The mass in hilum pulmonis depressed the heart. The cat died 9 days after the first medical examination.
The resected intra-abdominal and lung masses were fixed in 10% neutral-buffered formalin and embedded in paraffin. Sections were stained with HE and Masson trichrome. Using the streptavidin-biotin method, we performed immunohistochemical staining with the following primary antibodies: AE1/AE3 cytokeratin monoclonal antibody (DakoCytomation N1590, Dako, Kyoto, Japan); vimentin monoclonal antibody (DakoCytomation M0725, Dako); desmin polyclonal antibody (DakoCytomation A0611, Dako); alpha-smooth muscle actin (SMA) monoclonal antibody (DakoCytomation M0851, Dako); estrogen receptor (ER) monoclonal antibody (Novocastra NCL-ER-6F11, Vision Systems Inc., Norwell, MA) and caldesmon monoclonal antibody (Novocastra NCL-CALD, Vision Systems Inc.). A normal feline uterus was used as a positive control of these immunostains.
Grossly, the intra-abdominal mass measured 5.5 x 4.5 x 3.0 cm, was grayish-white on the cut surface, and was contiguous to a portion of the uterus (Fig. 1). Many grayish-white nodules 0.1–1.2 cm in diameter were observed in the lungs. There were no gross changes in the ovaries and mammary glands.
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Immunohistochemical staining with vimentin antibody was strongly positive on the spindle-shaped cells and stromal cells, whereas the tumor cells of the endometrial glands did not react to the antibody. The spindle-shaped cells and half of the stromal-like cells reacted to caldesmon and desmin antibodies, but glandular cells were negative (Fig. 4). Morphologic differentiation between smooth muscle cells and endometrial stromal cells was ambiguous in some areas. Therefore, the cells positive to desmin and Caldesmon antibodies were regarded as the neoplastic cells differentiated from smooth muscle cells. The neoplastic epithelium showing glandular formation expressed AE1/AE3 cytokeratin (Fig. 5). All types of tumor cells did not react to the SMA and ER antibodies. The same immunostaining profiles were obtained from both the intra-abdominal and lung masses (Table).
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Because the single abdominal mass arose from the endometrium, it was definitely from the uterus. A continuity between the mass and uterine wall grossly and microscopically was confirmed. The typical morphology of tumor cells resembling stromal cells and the presence of many arterioles were in agreement with characteristic features in human endometrial stromal sarcoma.1,2,4,8,9,12 In addition, a well-differentiated glandular formation is apparent evidence of the endometrial stromal origin. It has been known that the formation of glands or tubules may be present in low-grade endometrial stromal sarcoma in human patients.3,8 The hematogenous metastasis sometimes occurs in human endometrial stromal sarcomas, developing in 12 of 182 patients.5 Like high-grade endometrial stromal sarcoma, low-grade sarcoma can metastasize in human patients.4 The tumor definitely had malignant features such as local invasion and pulmonary metastases but did not apparently have malignant morphology because it had no mitotic index, as well as moderate nuclear pleomorphism and well-differentiated glands. Norris and Taylor8 have proposed that tubular formations and uniformed cells indicate low-grade endometrial stromal sarcoma.8 Our case had malignant biologic behavior but may be classified as a low-grade tumor.
Immunohistochemical examination successfully differentiated among the components of the normal feline uterus. The glandular epithelium reacted to AE1/AE3 cytokeratin, and the other tissues reacted to the vimentin. The smooth muscle cells in the myometrium reacted to the desmin, SMA, and caldesmon antibodies, as well as the vascular smooth muscle cells. The nuclei of the glandular epithelium, smooth muscle cells, and endometrial stromal cells reacted to ER antibody. A distinction between endometrial stromal tumor and smooth muscle tumor is always challenging in human patients because the immunohistochemical profiles of these tumors can overlap.2,10 Morphologically, typical smooth muscle cells always reacted to vimentin, desmin, and caldesmon antibodies; thus, they do not pose a diagnostic problem. However, with spindle-shaped cells in some areas, it was difficult to differentiate stromal cells from smooth muscle cells on HE stain.
A lack of desmin expression is sufficient to support endometrial stromal cells, but desmin expression is insufficient to exclude endometrial stromal tumors.11 In fact, half of the tumor cells showing desmin and Caldesmon expression in our patients apparently indicated the smooth muscle differentiation, although it is difficult to explain the lack of SMA expression. Interestingly, the neoplastic epithelium showing glandular formation expressed only AE1/AE3 cytokeratin, but not vimentin, desmin and Caldesmon. The CD10 antibody is known to be a positive marker for endometrial stromal tumor in humans.10 We used the CD10 monoclonal antibody (Novocastra NCL-CD10, Vision Systems Inc.) to differentiate from smooth muscle cells. However, the staining was nonspecific on feline tissue as well as progesterone receptors (Novocastra NCL-PGR-AB, Vision Systems Inc.).
McCluggage et al.7 reported human endometrial stromal sarcoma with smooth muscle and glandular differentiation as a unique variant that was similar to our case. It is still unknown whether our case has typical features of feline endometrial stromal tumor histologically and immunohistochemically. It is necessary to investigate more cases to design a classification outline of endometrial stromal tumor, but this report may serve as a first case of feline endometrial stromal sarcoma.
References
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