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ISSN : 1976-7447(Print)
ISSN : 2287-7363(Online)
Journal of Biomedical Research Vol.14 No.1 pp.47-50
DOI : https://doi.org/10.12729/jbr.2013.14.1.47

Chronic pyometra due to bilateral ovarian tumors in a South American sea lion

Kyu-Shik Jeong1,3,*, HaiJie Yang1,2, Sun-Hee Do1,4, Eun-Mi Lee1,3, Ah-Young Kim1,3, Eun-Joo Lee1,3, Chang-Woo Min1,3, Kyung-Ku Kang1,3, Myeong-Mi Lee1,3
1Department of Veterinary Pathology, College of Veterinary Medicine, Kyungpook National University, Daegu 702-701, Korea
2Institute of Natural Medicine, College of Medicine, Hallym University, Chunchon 200-702, Korea
3Stem Cell Therapeutic Research Institute, Kyungpook National University, Daegu 702-701, Korea
4Department of Clinical Pathology, College of Veterinary Medicine, Konkuk University, Seoul 143-701, Korea
Received 2 Feb. 2013, Revised 6 Mar. 2013, Accepted 11 Mar. 2013

Abstract

A 14-year-old female South American sea lion (Otaria byronia) with persistent vaginal secretion and chronic hemorrhagic diarrhea was encountered. During postmortem examination, the uterus was found to resemble a balloon with mucosal congestion and was filled with grayish milky material. The ovaries also had abnormal features, including necrotic surface lesions and multiple whitish foci in the cut section. Hemorrhages and ulcerated changes due to toxemia were observed in other organs, including the liver, spleen, lung, intestines, and lymph nodes. Microscopically, the left ovary contained interlacing fascicles of fibroblast-like cells with blunt-end nuclei showing cytoplasmic positive immunoreactivity against alpha-smooth muscle actin and desmin. The right ovary contained cells with round to cigar-shaped nuclei showing cytoplasmic positive immunoreactivity against vimentin. In conclusion, based on classification of bilateral ovarian tumors as a leiomyoma in the left region and a fibroma in the right region, this sea lion was diagnosed with chronic closed pyometra.

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Introduction

Pyometra is acute or chronic suppurative inflammation of the uterus with accumulation of large quantities of pus in the uterine cavity. This condition is observed with some frequency in bitches, queens, cows, and mares [1]. In general, it results from the persistence of an unresolved, nonspecific bacterial infection during periods of prolonged or excessive progesterone stimulation [2]. Escherichia coli is the most common bacterium isolated from cases of pyometra along with Staphylococcus, Streptococcus, Pseudomonas, and Proteus species [3]. Pyometra most commonly develops in older females after many years of estrus cycling without pregnancy [3,4]. 

 In canines, cattle, and sheep, a progestogenated uterus is susceptible to infections [1] but this is rare in sea mammals. Sea mammals are susceptible to infections with Brucella ssp, Erysipelothrix, Leptospira, Mycobacterium, and Mycoplasma. Among these different microorganisms, Brucella ssp causes uterine infections that result in reproductive problems [5]. In 1996, a larger study examined 370 california sea lions (Z. californianus) and documented 66 cases (18% incidence) of suspected transitional-cell carcinoma, with wide-spread metastases similar to the cases previously reported [6], but to our knowledge this is the first report of an ovarian tumor and pyometra in a south american sea lion. Here, we describe a female South American sea lion diagnosed with pyometra cause by ovarian tumors.

Case

 A 14-year-old female South American sea lion (Otaria byronyia) from a nearby commercial aquarium was presented to the College of Veterinary Medicine, Kyungpook National University with persistent vaginal secretion and chronic hemorrhagic diarrhea. Serum biochemical analyses revealed that this animal had metabolic acidosis, an electrolyte imbalance, and high levels of blood urea nitrogen (BUN), creatinine, bilirubin, and glutamate pyruvate transaminase (GPT). The sea lion died 7 days after and a necropsy was subsequently performed.

 All samples were fixed in 10% phosphate-buffered formaldehyde solution. Afterwards, the samples were embedded in paraffin and cut into 5-μm sections for histological staining with hematoxylin and eosin (H&E). For immunohistochemistry analysis, the sections were stained with primary antibodies specific for α-SMA (1:800 dilution; Sigma, St. Louis, MO, USA), S-100 (1:100 dilution; Santa Cruz, CA, USA), vimentin (1:100 dilution; Dako, Carpinteria, CA, USA), and desmin (1:100 dilution; Dako, Carpinteria, CA, USA). The antigen-antibody complex was visualized with avidinbiotin complex immunoperoxidase systems using a commercial kit (Vector Laboratories, Inc., Burlingame, CA, USA), with 3,3’-diaminobzidine (DAB; Zymed Laboratories Inc., San Francisco, CA, USA) by detection system, and counterstained with Mayer’s hematoxylin.

Discussion

 Grossly, the uterus of the sea lion resembled a balloon filled with grayish milky fluids, with an enlarged left horn and mucosal congestion. The solid right ovary contained a whitish gray tumor attached to the uterine ampulla area (Fig. 1A). On cut surfaces of the right ovary, a well encapsulated tumor-like lesion as well as other lesions with necrotic and fibrotic processes was observed. In the left ovary, whitish foci were found in the transmural cortex and medulla (Fig. 1B).

Fig. 1. Gross findings in the uterus and ovaries of the South American sea lion. (A) The sea lion uterus resembled a balloon filled with grayish milky fluids with an enlarged left horn (inset) and mucosal congestion. The solid right ovary (arrow head) contained a whitish gray tumor attached to the ampulla area of the uterus. Scale bar = 1 cm. (B) On cut surfaces of the right ovary, a well encapsulated tumor-like lesion (circled with a yellow line) as well as other lesions with necrotic and fibrotic processes were observed. The left ovary contained whitish foci in the transmural cortex and medulla. Scale bar = 1 cm.

 Microscopically, the uterus contained highly activated endometrium glands, necrosis of the myometrium circular, neovascularization, and bundles of eosinophlic endometrium (Fig. 2A). In the left ovary, cells with blunt-end nuclei formed interlacing fascicles running at various angles (Fig. 2B). Histological features characteristic of tumor cells in this mass concurred with immunohistochemical findings as shown in Figs. 2C-2F. The tumor cells were diffusely positive for α-SMA (Fig. 2C), desmin (Fig. 2D), vimentin (Fig. 2E), and S-100 (Fig. 2F).

Fig. 2. Histopathological and immunohistochemecal findings in the uterus and ovary. (A) The sea lion uterus contained highly activated endometrium glands, necrosis of the myometrium circular, neovascularization, and bundles of eosinophlic endometrium. H&E staining. Scale bar = 100 μm. (B) In the left ovary, cells with blunt-end nuclei formed interlacing fascicles running at various angles. H&E staining. Scale bar = 50 μm. (C) In the left ovary, tumor cells showed strong positive staining for α-SMA. Immunohistochemistry with hematoxylin counterstaining. Scale bar = 50 μm. (D) Tumor cells in the left ovary were positive for desmin. Immunohistochemistry with hematoxylin counterstaining. Scale bar = 50 μm. (E) In the right ovary, tumor cells were positive for vimentin. Immunohistochemistry with hematoxylin counterstaining. Scale bar = 50 μm. (F) Tumor cells in the right ovary showed positive staining for S-100. Immunohistochemistry with hematoxylin counterstaining. Scale bar = 50 μm.

 Epidemiological studies have indicated a relationship between gonadal steroid hormones and ovarian cancer [7]. Production of progesterone by ovarian cancers has been demonstrated [8, 9]. Furthermore, progesterone levels are significantly higher in all ovarian tumors whether they are malignant or benign [7]. If progesterone secretion is abnormally prolonged, cystic endometrial hyperplasia can develop [10]. Accumulation of uterine secretions may occur, which provide an excellent environment for bacterial growth. Progesterone may also inhibit the response of white blood cells against bacterial infection [11]. Normal vaginal bacteria or subclinical infection of the urinary tract are the most likely causes of pyometra.

In cases of open pyometra, the uterus contains pus with vaginal discharges that are often bloody. With closed pyometra, no discharge from the vagina is observed, and abdominal distention and pain may develop due to the uterus enlarged with pus [12]. Clinical signs of this type of pyometra can rapidly worsen, and lead to shock and death.

 The characteristic reproductive anatomy of female sea lion includes a genital lock system in the lower vagina. This genital lock is composed of folds of fibrous tissue, called hymeneal folds, which are located 4-6 cm from the entrance of the vagina. The hymeneal folds contain muscle cells that appear to constrict the entrance of the vagina. Presumably, the purpose of this genital lock is to contract the vaginal canal after intromission by the male, thereby excluding seawater, sand, pebbles, and debris during copulation, or to prevent the entry of seawater during diving [13]. This structure can make incidence of pyometra more severe in sea mammals.

 In summary, we have described the gross, histopathological, and immunochemical features of ovarian tumors and pyometra in a female South American sea lion. The left ovary tumor (determined to be a leiomyoma) arose from smooth muscles while the right ovary tumor was classified as a fibroma. We suspect that the bilateral ovarian tumors and infectious agent(s) cause a chronic case of closed pyometra due to an excessive quantity of progesterone.

Acknowledgements

This research was supported by the Kyungpook National University Research Fund, 2012. 

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