Ovarian remnant syndrome in a 5-year-old bitch

Abstract

A 5-year-old German shepherd bitch was presented with a 3-week history of vaginal bleeding. Ovarian remnant syndrome was diagnosed on vaginoscopy, vaginal cytology, serum progesterone levels, ultrasonography, and exploratory laparotomy. The condition resolved following surgical excision of the remaining ovarian tissue.

A 5-year-old, German shepherd bitch was presented to the Small Animal Clinic at the Western College of Veterinary Medicine with a 3-week history of bleeding from the vagina in the form of constant dark red drops. The owner had also noted swelling of the vulva and increased licking of this area by the dog. The owner claimed that swelling of the vulva had occurred intermittently since the dog had been spayed during its 1st y of life, but that the original clinic had not pursued the issue when presented with it. The owner had noticed no other changes in the dog’s behavior or health.

On physical examination, the animal was bright and alert. The vulva was approximately 3 × the expected size for a spayed bitch; a dark red fluid, presumed to be blood, was pooled at the ventral commissure; and the surrounding hair coat was dotted with blood. Multifocal areas of erythema were noted on the ventral aspect of the abdomen.

Further examination was facilitated by sedating the bitch with acepromazine (Atravet; Ayerst Veterinary Laboratories, Guelph, Ontario), 0.05 mg/kg bodyweight (BW), IM, and hydromorphone (WCVM Teaching Hospital, University of Saskatchewan, Saskatooon), 0.1 mg/kg BW, IM. Vaginoscopy was performed with the dog in sternal recumbency by using a vaginoscope to visualize the vestibule and distal vagina and a pediatric proctoscope to visualize the vagina to the level of the cervix. The epithelium had a cobblestone appearance; blood was noted in the vestibule and vagina, but it could not be localized to any particular site of trauma or a lesion. No evidence of a distinct mass was found. Visualization of the urethral papilla revealed no evidence of bleeding from the urinary tract. Catheterization was accomplished easily and grossly no blood was seen in the urine. Vaginal cytologic examination determined that cells were typical of a bitch in estrus. Biopsy samples of the vaginal mucosa were fixed in 10% neutral buffered formalin, but they were archived and not submitted for pathologic examination at that time. Abdominal ultrasonography revealed a hyperechoic area cranial to the right kidney that was interpreted to be a potential mass. Serum progesterone was 5 ng/mL (normal in a spayed bitch is < 0.2 ng/mL), indicating that ovulation had occurred.

Exploratory laparotomy was performed 3 wk later. No abnormal findings were noted on the presurgical complete blood (cell) count (CBC) and serum biochemical analysis. A protein value of 1 + and alkaline pH were noted on the presurgical urinalysis. An anesthesia pre-medicant of acepromazine (Atravet; Ayerst Veterinary Laboratories), 0.03 mg/kg BW, and hydromorphone (WCVM Teaching Hospital), 0.1 mg/kg BW was administered, IM. Induction consisted of propofol (Abbott Laboratories, Saint Laurent, Quebec), 60 mg, IV; anesthesia was maintained with inhalational isoflurane and nitrous oxide gas. Cefazolin (Cefazolin; Novopharm, Toronto, Ontario), 22 mg/kg BW, was administered intraoperatively and meloxicam (Metacam; Boehringer Inglehiem, Burlington, Ontario), 0.2 mg/kg BW, SC, was administered at the time of induction for pain control. A 3-cm mass was found attached to the caudoventral peritoneal surface of the right kidney. It was bluntly dissected from the peritoneum, isolating a single vascular pedicle, which was ligated with 1 transfixation and 1 circumferential ligature, and then transected. No abnormal tissue was detected on the left side of the abdomen. The uterine stump was moderately enlarged, but all other abdominal organs appeared normal. The abdomen was flushed with 1.0 L of warm saline and then closed. The excised tissue was submitted for histological evaluation. Serum progesterone the following day was 0.39 ng/mL.

The staples were removed 2 wk later, when the suture line was noted to be healing well. Serum progesterone at this time was <0.2 ng/mL.

Gross evaluation of the excised tissue revealed an encapsulated, lobulated mass that was firm and tan/white on cut section. Microscopically, it contained epithelial structures very reminiscent of ovarian follicle formation, cuboidal to columnar epithelium forming circular to oval structures surrounding a vacuolated space in some areas and stratified to pseudostratified layers of columnar cells with vacuolated cytoplasm forming elongated or oval structures in others. Primordial, primary, or further follicular development could not be identified, and no oocytes were noted. Most of the tissue in the mass was stromal and there was no appearance of neoplastic tissue.

Signs of estrus in the bitch include bleeding from the vagina, a cobblestone or crepe paper appearance to the vaginal epithelium, and the presence of largely or wholly cornified superficial cells on vaginal cytologic examination (1). Ovulation occurs near the beginning of estrus in the bitch and is indicated by a serum progesterone level between 3 and 8 ng/mL (1). In this case, these signs in a spayed bitch led to a presumptive diagnosis of ovarian remnant syndrome. Discovery of a mass on ultrasonography and exploratory laparotomy were consistent with this diagnosis and the histologic examination provided confirmation.

Ovarian remnant syndrome is defined as “the presence of functional ovarian tissue in a previously ovariohysterectomized bitch or queen” (2). The clinical presentation is characterized by signs of proestrus and estrus, including vulvar swelling; bloody vaginal discharge; and behavioral changes, such as flagging. Some animals may even allow copulation, but they do not become pregnant (2). In dogs, onset of these signs has been reported between 2 wk and 3 y from the time of the original ovariohysterectomy (3). The cause of this syndrome is ovarian tissue left in the abdomen following ovariohysterectomy. This can occur in the dog as a result of improper placement of clamps or ligatures, poor visualization of the surgical field, or revascularization of a piece of ovarian cortex dropped into the abdomen during surgery (2). Ectopic ovaries have not been reported and accessory ovaries have only been reported in cats, cows, and humans (3). In a review of complications of ovariohysterectomy, ovarian remnant syndrome was found to occur in 12 of 72 cases (17%) (4). No association has been found between the syndrome and difficult ovariohysterectomies, such as in overweight or deep-chested dogs, or animals with pyometra (2). There also does not appear to be an association with lack of experience, as 1 study found that fewer than half of the cases reviewed had been operated on by new graduates (received DVM degree < than 5 y previously) (5).

Four methods have been suggested to diagnose ovarian remnant syndrome: vaginal cytologic evaluation, resting hormone assays, hormone challenge testing, and exploratory laparotomy with biopsy (2). Ultrasonography of the abdomen can add further evidence that an ovarian remnant is present. Due to the estrogen produced by the remnant, vaginal cytologic examination may reveal cornified epithelial cells (3). An estrodiol concentration of > 20 pg/mL can be considered as evidence of ovarian remnant syndrome, but it is not thought to be as reliable as progesterone measurements. Progesterone should be measured when the bitch is showing signs of estrus or within 50 to 80 d after that with a level > 2 ng/mL indicative of functional corpora lutea (2). A hormone challenge test is more reliable in the queen, but it can be used in the bitch if a progesterone level of < 2 ng/mL is found, or the animal is presumed to be in proestrus. Progesterone levels should increase to > 2 ng/mL by 1 wk following the injection of human chorionic gonadotropin or gonadotropin releasing hormone (3). Confirmation of the diagnosis can only be made by exploratory laparotomy and histological confirmation of the presence of ovarian structures in conjunction with resolution of the signs (2).

Exploratory laparotomy and excision of the remnant is also the treatment of choice. The surgery should take place during estrus, as the residual tissue may be easier to find at that time. Difficulty in finding the remnant may still occur, when enlarged ovarian vessels may aid in determining on which side the tissue remains (3). If it cannot be determined on which side the remnant lies, the granulation tissue at each ovarian pedicle should be removed and the pedicle itself should be clamped, ligated, and severed closer to the aorta (2,3). Excised tissue should always be submitted for histological examination (3).

Complications of ovarian remnant syndrome include the formation of granulosa cell tumors, uterine stump pyometra, and mammary neoplasia; thus surgical excision of the ovarian remnants should be highly recommended (2,6). Granulosa cell tumors can also secrete estrogens and progesterones, resulting in the same clinical signs as ovarian remnant syndrome (6). Though formation of the tumor may induce the onset of the clinical signs, these tumors will only form if an ovarian remnant or accessory ovarian tissue, which has never been reported in dogs, remains in the animal. Eighty percent of granulosa cell tumors are considered to be benign and usually do not spread by direct extension or metastasis (7). Therefore, removal of the tissue will typically be curative.

Although identified as a syndrome, ovarian remnant syndrome is an iatrogenic condition that can be prevented through careful and proper surgical technique. When presented with a spayed animal showing signs of estrus, a series of diagnostic tests culminating in exploratory laparotomy and excision of the remnant tissue is recommended.