History

An 8-year-old 719-kg maiden warmblood mare was presented to the Cornell University Equine and Nemo Farm Animal Hospital for right-sided ovarian enlargement, which was an incidental finding during examination for transvaginal aspiration (TVA) for oocyte recovery. The mare was part of the Cornell University Equine Park teaching and research herd and had previously been used for transvaginal luteal biopsy (TVLB) research. The luteal biopsy samples were retrieved using an ultrasound-guided luteal biopsy device in July 2020 (right ovary), June 2021 (left ovary), and again in August 2021 (right ovary). The last sampling period involved taking 5 biopsy samples on 2 sampling dates (day 11 and 13 after ovulation). As part of the research protocol, on the last day of sampling, the mare received flunixin meglumine (1.1 mg/kg, IV, once) and had rectal temperature monitoring for the 3 subsequent days. The mare remained afebrile during the 3-day period. No antimicrobials were given as part of this research protocol, and the mare was returned to routine turnout with pasture mates.

On February 8, 2022 (6 months after last TVLB), during the mare’s reproductive examination to determine candidacy for TVA, transrectal palpation revealed right ovarian enlargement and lobulation, with mobilization being extremely difficult. On transrectal ultrasonography, there were areas of increased homogenous echogenicity resembling luteal tissue or an anovulatory hemorrhagic follicle. The left ovary was used for TVA, and the mare was given 4 weeks of rest. The mare was reevaluated after the rest period, and ultrasonography revealed that the densely echogenic areas of the right ovary had not changed in size, but a week later, they appeared to be developing a focal area of hypoechogenic material deep within the center (Figure 1).

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Serial transrectal ultrasonographic images of the right ovary of an 8-year-old 719-kg maiden warmblood mare with right-sided ovarian enlargement 6 months (A), 7 months (B), and 8.25 months (C) after transvaginal ultrasound-guided luteal biopsy. A—There is a structure (white arrow) that resembles an anovulatory hemorrhagic follicle or more homogeneous structure. B—Echogenicity of the same structure (dashed arrow) has changed to be more heterogeneous. C—A focal hypoechoic region (white asterisk) surrounded by heterogeneous echotexture (white arrowhead), consistent with an abscess, is present.

Citation: Journal of the American Veterinary Medical Association 261, 4; 10.2460/javma.22.12.0561

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Diagnosis

Due to unilateral ovarian enlargement, hormone testing, including concentrations of anti-Müllerian hormone (AMH), testosterone, and inhibin, was performed. The hormonal assays for granulosa cell tumor (GCT) were within reference limits, with concentrations of AMH at 0.51 ng/mL (reference range, 0.1 to 6.9 ng/mL), inhibin at < 6 ng/mL (reference range, 2 to 100 ng/mL), and testosterone at < 0.01 ng/mL (mare reference limit, < 0.01 ng/mL). Given the young age of the mare, the history of TVLB, and the ultrasonographic appearance of the right ovary, suspicion for ovarian abscess was the top differential diagnosis. A standing laparoscopic bilateral ovariectomy (OVE) was elected, with the intent of future use as a tease mare for stallion collections.

On March 21, 2022, the mare was transported to the Equine and Nemo Farm Animal Hospital for surgery. Following premedication with systemic antimicrobials and anti-inflammatory medication, the mare’s left and right paralumbar fossae were clipped and prepared for routine OVE. The left ovary was visualized, lidocaine was injected into the mesovarium with a laparoscopic needle, and a blunt-tip vessel sealer (LigaSure; Covidien-Medtronic) was used to transect the mesovarium, mesosalpinx, and proper ligament of the ovary. The procedure was then repeated for the right ovary. Upon amputation of the right ovarian tissue, it was discovered that the ovary was too large to be removed, so a right-sided large flank incision was made to facilitate removal of the ovary. At this point, the ovary was suspected to be adhered to the large colon and could not be removed laparoscopically. The decision was made to induce general anesthesia and approach the ovary from a ventral midline incision. The following day, the mare was anesthetized and placed in dorsal recumbency, and a ventral midline approach was used to enter the abdominal cavity to exteriorize the section of colon where the ovary was attached. Due to the degree of adhesion to the left dorsal and ventral colon, a resection with hand-sewn anastomosis was performed.¹ The mare recovered from anesthesia without any complications. The ovary—with adhered segment of colon—was submitted for histopathology and bacterial culture at the Cornell Animal Health and Diagnostic Center (Figure 2).

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The ex situ resected segment of colon and the right ovary of the mare described in Figure 1. A—Firm adhesions (pound sign) span between the colon (brackets) and right ovary (arrows), and the latter is substantially enlarged and has abundant serosal hemorrhage (arrowhead). B—On cut surface, the right ovary has massive parenchymal effacement, with multifocal aggregates of thick, opaque liquid to semisolid friable, purulent material (solid arrows), and is boarded by dense, pale tan fibrotic tissue (arrowheads) and dark red granulation tissue (dashed arrows). The scales in the lower right of each image are in centimeters.

Citation: Journal of the American Veterinary Medical Association 261, 4; 10.2460/javma.22.12.0561

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The right ovary measured approximately 16 X 16 X 10 cm and had a dark red serosal surface. On cut surface, most of the ovarian parenchyma was effaced by multifocal to coalescing aggregates of thick, opaque, liquid to semisolid friable material, surrounded by firm, pale tan tissue (Figure 2). Microscopically, multifocally replacing the ovarian stroma were large, coalescing pools of degenerate neutrophils—sometimes interspersed with bacterial colonies—rimmed by hemorrhage and fibrin and encapsulated by richly vascular fibrous granulation tissue. Dense fibrous connective tissue replaced much of the periovarian adipose tissue, consistent with fibrosis. Within remaining ovarian stroma, vessels were often cuffed by lymphocytes, plasma cells, and fewer macrophages.

Routine aerobic bacterial culture of ovarian samples resulted in growth of Streptococcus equi subsp zooepidemicus. Gram-stained histologic sections of the right ovary revealed a mixed population of bacteria strewn among the neutrophilic and cellular debris, including small gram-negative cocci, small gram-negative coccobacilli, small gram-positive cocci, and large gram-positive cocci. This finding was most compatible with contamination from a TVA procedure, rather than a hematogenous route of infection. The final diagnosis was right ovarian abscess, with hemorrhage, granulation tissue, fibrosis, and polymicrobial infection.

Treatment and Outcome

This patient spent 8 days in the hospital and finished the recovery period with stall confinement followed by gradual increases in length of turnout. The mare exhibited signs of 1 bout of colic 2 weeks postoperatively and was hospitalized for 3 days. The mare received medical management consisting of IV fluids and pain management and recovered quickly.

Discussion

The differential diagnoses for ovarian enlargement in the mare include tumors, persistent anovulatory follicles, ovarian hematoma, multiple corpora lutea of pregnancy, adjacent ovarian embryological origin remnants, and ovarian abscess.² The most common equine ovarian tumor is GCT, or granulosa-theca cell tumor, if theca cells are also involved. These are sex cord stromal tumors, with other less common examples including thecoma and luteoma. Other ovarian tumors in the mare include germ cell tumors (eg, dysgerminoma and teratoma) and tumors derived from the ovarian epithelium (eg, serous cystadenoma).² The typical presentation of a GCT is a unilaterally enlarged ovary with distinct multifollicular or polycystic honeycombed areas, with solid areas of parenchyma and a lack of discernable ovulatory fossa on transrectal palpation, and with accompanying contralateral ovarian inactivity.² Usually there are behavioral issues leading to diagnosis, and hormonal biomarkers such as AMH, inhibin, and testosterone are typically increased.² Due to the history of transvaginal ultrasound-guided luteal biopsy on the affected ovary 6 months prior, the low concentrations of all of the hormonal biomarkers, and the normal contralateral ovary in this case, GCT was ruled out and ovarian abscess was suspected, with the latter subsequently being confirmed with gross evaluation and histopathology.

Transvaginal oocyte aspiration has gained popularity over the past several years to increase the ability to produce a foal from subfertile mares or stallions with decreased semen availability through intracytoplasmic sperm injection. Complications from TVA are rare but have been previously reported, such as when Velez et al³ reported that < 0.5% (1/390) of mares developed complications such as ovarian abscess, with the most common complication noted being minor rectal irritation and bleeding during manipulation of the ovaries, causing no long-term effect on ovarian function or fertility. TVLB was first reported in a mare by Beg et al,⁴ to look at luteal mRNA. Additionally, further research that enrolled 53 mares and involved 183 transvaginal ovarian and/or luteal biopsy procedures found no effect of the TVLB on mare fertility and reported no serious complications besides minimal rectal mucosal bleeding,⁵ similar to the findings of Velez et al.³ To our knowledge, the present report is the first of an ovarian abscess with subsequent adhesion to the left dorsal colon as a complication after TVLB. This complication was only discovered incidentally during transrectal ultrasonography 6 months following the procedure. The mare was not noted to have any change in demeanor and had not shown signs of colic during those months. It is suspected that there was inadvertent biopsy needle device contamination that seeded bacteria into the right ovary during the TVLB procedure, which led to abscess formation. This in turn led to serosal adhesion between the right ovary and the left ventral and dorsal colon, which is mobile in the horse. Standing laparoscopic surgery has led to greater efficiency in performing OVE in horses, with a reduced recovery time. The aim of this procedure is to have better visualization and to enable resection of the ovarian pedicles in situ. Colectomies, such as the one performed in the case reported here, are used as a salvage or prophylaxis procedure and have a rate of survival to hospital discharge of 86% (12/14) with the hand-sewn anastomosis technique, with approximately 50% (13/26) experiencing another bout of colic within 1 year.¹

Outcome

The mare subsequently returned to its herd and has continued to contribute to the veterinary teaching curriculum, now at 8 months after surgery.