Tératome ovarien et endométrite chez une jument. Une jument Arabe de 8 ans fut présentée pour un gros ovaire. Un diagnostic de tumeur ovarienne et d’endométrite fut posé. L’examen histologique confirma un tératoma ovarien et une endométrite grade II. Trois mois après une ovariectomie unilaterale, la jument fut diagnostiquée gravide et mit bas sans assistance.

(Traduit par les auteurs)

An 8-year-old Arabian mare was presented in June 1999 to the Centre Hospitalier Universitaire Vétérianaire (CHUV), University of Montreal, with the complaint of a persistent anovulatory follicle and infertility. The mare was otherwise healthy; regularly vaccinated and dewormed; and without a history of trauma or disease. Results from a physical examination, a complete blood (cell) count (CBC), and routine blood serum biochemical analyses were normal.

The mare had foaled normally 3 mo earlier and her 1st postpartum estrus (foal heat) was described as normal, except that the referring veterinarian had palpated a large follicle on the right ovary that persisted in subsequent estrous cycles. Despite the ovarian anomaly, the mare had cycled normally with ovulation being confirmed ultrasonographically. She was artificially inseminated twice with extended semen at each of the 3 subsequent estrous periods, without conceiving. The most recent insemination had taken place 9 d prior to referral.

The perineal angulation and the dorsal commissure of the vulva were normal, and no vulvar discharge was noticed. On transrectal palpation, the cervix was tubular, regular in size, and relatively firm, while the uterus was normal in size and had moderate tone, without detectable endometrial folds, which was compatible with a mare in diestrus. The right ovary had a large, round structure with a smooth surface, while the left ovary appeared normal in size and consistency. Ultrasonographic (Aloka, 210DX; ISM, Montreal, Quebec) examination of the uterus, using a 5 MHz linear probe, did not reveal any remarkable changes. However, the right ovary showed a follicle-like-structure, 6 to 7 cm in diameter, that contained several round hyperechoic structures of 1 to 1.5 cm diameter (Figure 1). Several follicles (1 to 2 cm diameter) were found adjacent to this structure. The left ovary had a corpus luteum (CL), 2.5 cm in diameter. The CL was confirmed by radioimmunoassay, which showed a progesterone (P4) level of 4 ng/mL of serum. On day 14 postovulation (6 d postreferral), the mare was confirmed as being open by ultrasonographic examination of the uterus showing the absence of an embryonic vesicle, while the appearance of both ovaries and the uterus was similar to that noted on initial assessment. The diagnostic plan was to assess the structure of the right ovary, as well as the return to estrus, and to investigate the genital condition of the uterus (biopsy, culture, and endometrial cytologic examination).

Figure 1 Ultrasonographic image of the mass of the right ovary, which appeared anechoic, like a large follicle containing several echoic structures of 1.0 to 1.5 cm diameter.

During estrus, ovaries were monitored by transrectal palpation and ultrasonographic examination. Over a 10-day period, the follicle-like structure containing several echoic structures persisted and the preovulatory follicle on the left ovary did not ovulate. Endometrial biopsy and cytologic examination were performed during estrus to determine the condition of the endometrium. The cytologic findings were negative, while bacteriologic cultures showed occasional colonies of Streptococcus zooepidemicus. On histopathologic examination, the surface and glandular epithelial cells were columnar, reflecting estrus. Small foci of lymphocytes, accompanied by occasional neutrophils and eosinophils but numerous hemosiderin-laden macrophages, were scattered throughout the stratum compactum and spongiosum. Endometrial glands were numerous and tortuous, and their lumens were empty. Mild fibrosis (1 layer thick) was observed around some uterine glands and blood vessels (Figure 2). The endometrial changes were characterized as a grade II endometritis, based on Kenney’s classification (3). After surgery and following a 5-day treatment consisting of an intrauterine infusion of 50 mL of procaine penicillin G (Ethacilin, 300 000 IU/mL; Pfizer Canada, Montreal, Québec), q24h for 5 d, the uterine infection resolved.

Figure 2 Histopathological changes of the reproductive tract. Lymphocytes and hemosiderin-laden macrophages were scattered throughout the stratum compactum and spongiosum; grade II endometritis (Bar = 100 μm).

Because of the persistence of a follicle-like structure with an unusual echotexture on the right ovary, the palpation of 2 small (15 to 17 mm) very firm masses (bony texture) on the dorsal aspect of the right ovary, and the growing mass that could potentially affect the normal ovarian physiology (nonovulation during the last estrus period), the right ovary was removed surgically. The surgery was done by a flank grid approach with the mare in left lateral recumbency under general inhalation anesthesia. The right ovary was exteriorized to allow placement of a transfixation ligature on the mesovarium and then removed. In postsurgical care, procaine penicillin G (Ethacillin), 20 000 IU/kg BW, IM, q24h for 2 d was administered, followed by ceftiofur sodium (Excenel; Pharmacia Animal Health, Orangeville, Ontario), 2.2 mg/kg BW, IM, q24h for 5 d. Then flunixin meglumine (Flunazine; Bimeda-MTC, Animal Health, Cambridge, Ontario), 1 mg/kg BW, IM, was given q12h for 3 d, followed by phenylbutazone (Phenylbutazone; Univet Pharmaceuticals, Milton, Ontario), 2.2 mg/kg, BW, PO, q12h for 5 additional days. Light exercise was restored 14 d after surgery and full exercise resumed 6 wk later.

The estrous cycle resumed 45 d after the unilateral ovariectomy and the endometritis treatment. Insemination was planned for the 2nd estrus, in view of the uterine condition, which may favor breakdown of normal uterine defense mechanisms, only 1 insemination with extended fresh semen from a stallion with known fertility was performed. Follicular growth was monitored and ovulation of the preovulatory follicle (3.5 cm in diameter) was induced with 2500 IU of human chorionic gonadotropin (Chorulon; Intervet Canada, Whitby, Ontario). Uterine lavage with 2.0 L of sterile saline was performed 24 h after insemination, followed by an oxytocin treatment (15 IU, IV).

On macroscopic examination, the right ovary presented a firm, lobulated surface (Figure 3), as well as fibrous adhesions to the ovarian bursa. On cross section, the lobules corresponded to hair-filled cysts lined with cartilage (Figure 4). Histologically, various tissues, such as epithelium, muscle, and cartilage from different germ layers (embryonic origin), were observed, together with numerous cysts (Figure 5A). Some of the cysts were lined by skin that displayed a well-differentiated keratinized, stratified squamous epithelium, sebaceous glands, and hair follicles (Figure 5B). Other cysts were lined with ciliated respiratory epithelium and were often surrounded by rings of cartilage (Figure 5B). Areas of smooth muscle, adipose tissue, and blood vessels, as well as undifferentiated mesenchymal tissue, were also present. Based on its histological appearance, the mass was diagnosed as an ovarian teratoma.

Figure 3 Macroscopic appearance of the right ovary. Presence of a large, round, and smooth follicle (a) on the right ovary, which corroborated the transrectal palpation findings.

Figure 4 On cross section of the right ovary, multiple small follicles (b) and the large follicle (a) with hair balls and several masses of cartilage of 1.0 to 1.5 cm of diameter can be observed.

Figure 5 (A) Cysts lined by a ciliated respiratory epithelium and surrounded by cartilage were present in the ovarian mass (Bar = 50 μm). (B) Areas of stratified squamous epithelium, sebaceous glands, and hair follicles were also observed in the (more ...)

Differential diagnoses for an enlarged ovary should include nonneoplastic conditions (anovulatory follicle, ovarian hematoma, ovarian abscess), as well as neoplastic conditions (GTCT, teratoma, dysgerminoma, and lymphosarcoma).

Anovulatory follicles are the primary cause of large ovaries (4). The condition is most apparent during the transitional period (spring or fall), when the mare exhibits irregular signs of estrus, but it is considered abnormal during the ovulatory season (4). Throughout most of the transitional phase, mares remain anovulatory, despite continued development of large follicles (6). In the present case, the ultrasonographic examination was not consistent with an anovulatory follicle (no large follicles on the ovaries; presence of a CL) and the reproductive history (regular estrus) suggested that the mare had resumed her normal breeding season. In hospital, monitoring of a complete estrus cycle ruled out of an anovulatory follicle.

Ovarian hematomas in the mare are usually quite large. On ultrasonographic examination the blood-filled follicle initially appears hypoechoic, then, as the blood clot becomes more organized, the appearance is mottled. The ovary may take months to return to normal size and echogenicity; however, hematomas are not always associated with infertility (5). In the present case, the ultrasonographic examination was not consistent with a hematoma.

Ovarian abscesses are usually unilateral and ultrasonography is undoubtedly the most accurate diagnostic tool to differentiate an abscess from other ovarian conditions. In contrast to the case described herein, an abscess usually presents a homogeneous hyperechoic appearance surrounded by a thick wall.

Ovarian tumorigenesis is rare in the horse. Tumors arising from ovarian tissues are classified according to their cellular origin (7): 1) germinal epithelium; 2) sex cord stromal; and 3) germ cell (Table 1). In the first category, tumors such as adenomas and adenocarcinomas arise from the ovarian surface epithelium. Since they are nonsecretory, they do not incite behavioral changes and the mare continues to cycle normally and ovulate from the unaffected ovary. Conversely, tumors of the sex cord and ovarian stroma secrete several hormones, including progesterone (P4), estradiol (E17b), and testosterone (T). In this category, the GTCT is the most commonly reported ovarian tumor (1). Granulosa and theca cells usually coexist in the same neoplasm and produce different hormones, varying the clinical characteristics of the condition. The high levels of inhibin, which inhibits release of follicule-stimulating hormone (8), then alter the normal ovarian cycle and provoke anestrus. Estrogens cause continuous or intermittent estrus, while androgens, such as T, will stimulate stallion-like behavior, including aggressiveness, mounting, and squealing. In more than 50% of GTCT, serum T concentrations will exceed 70 pg/mL (9), while stallion-like behavior is generally associated with a concentration of T greater than 100 pg/mL (10). In the present case, no behavioral modifications had been observed by the owner and no typical ovarian changes, such as atrophy of the contralateral ovary in relation to the presence of steroid hormones or inhibin (11), were noticed upon transrectal palpation. The dysgerminoma, an ovarian tumor arising from germ cells, is highly malignant, commonly leading to infertility (12) and loss of general condition (13,14). In the present case, infertility was more likely associated with the grade II endometritis than with the ovarian abnormality. While the teratoma is considered the second most frequently seen ovarian tumor in horses, it is a very rare condition. A 2-year survey performed on 1380 abattoir horses revealed only 1 case of teratoma and it affected the testis (15). Likewise, in the past 15 y, only 3 other cases have been presented to Canadian veterinary schools, all of them in stallions (personal communication: Spencer Barber, WCVM; Antonio Cruz, OVC; Christopher Riley, AVC). Between 1983 and 2003, the present case was the only teratoma diagnosed at the CHUV. During the same period, 8 GTCT were diagnosed and treated surgically, while a total of 1683 mares were examined for other reproductive problems. Of the 5 cases of equine ovarian teratoma reported in the literature, 3 mares were Arabian and all were nulliparous (16–18). Catone et al (19) described the clinicopathological features of an ovarian teratoma in an Andalusian mare. The mare described in this report was also of Arabian breed, but she had foaled prior to presentation. Because the number of cases is so small, it is difficult to draw any conclusion about breed predilection.

Table 1 Classification of ovarian tumors according to their frequency, malignancy, secretory function, and tissue of origin

The fact that the mare had regular estrous cycles before referral is not surprising, because a teratoma, like other nonfunctional ovarian tumors, does not produce hormones that negatively affect reproductive physiology. The present mare did not ovulate during the last estrus while hospitalized; however, normal estrous cycles resumed in a short period after discharge. Teratomas are diagnosed incidentally during a routine examination of the reproductive system. Although normally developing follicles reach 4 to 5 cm in diameter during the breeding season, an enlarged ovary in the mare is described as having a diameter exceeding 10 to 12 cm (4). Ultrasonography is very useful to determine the stage of the estrous cycle, to assess the status and the number of preovulatory follicles, to characterize the developing CL, and, finally, to assist in the diagnosis of ovarian irregularities. Although the aforementioned types of ovarian tumors differ in their clinical and ultrasonographic characteristics, more than 1 type can coexist in the same animal (16).

Because of the low number of cases, it is difficult to prognosticate on long-term outcome; however, taking into account the teratoma’s characteristics, fertility and survival rates should compare favorably with those following any other elective abdominal surgery. The grade II endometritis of the present mare carries a 50% to 80% expected foaling rate (20). The clinical interest of this case lies in the difficulty to differentiate an ovarian teratoma from other conditions affecting the ovaries and the relative infertility that could be associated with it. A complete reproductive history and a series of transrectal and ultrasonographic examinations over a certain period of time might be necessary to establish a presumptive clinical diagnosis. For final diagnosis, histopathological examination of the ovarian tissue is necessary. CVJ