A 23-year-old Quarter Horse mare (mare 1) weighing 494.45 kg (1,090 lb) was admitted to the Texas A&M University Veterinary Medical Teaching Hospital because of infertility. The mare was used exclusively as an embryo donor and had produced 18 foals previously. Palpation per rectum of the reproductive tract revealed a markedly distended uterus with normal-sized ovaries. Transrectal ultrasonography confirmed a large amount of echogenic fluid within the uterus. The degree of uterine distention prohibited complete measurement of the uterine body and horns, although the dorsal aspect of the uterine wall was > 2 cm thick in both horns and the body. Vaginal speculum and digital cervical examination revealed a fibrous, distorted cervix with transluminal adhesions that was obstructive and precluded cervical patency. Pyometra secondary to transluminal cervical adhesions was diagnosed.
The purulent material was removed from the uterus over a period of days in an effort to reduce potential contamination during cervical surgery. The mare was restrained in a set of stocks with the tail wrapped and reflected to the side. Sedation was provided by administration of detomidine hydrochloride (0.01 mg/kg [0.0045 mg/lb], IV) and butorphanol tartrate (0.01 mg/kg, IV). The perineum was aseptically prepared with povidone-iodine scrub and water. A sterile vaginal speculum was placed to view the cervix. Subsequently, the cervix was digitally palpated and the presence of the adhesions was confirmed. Adhesions were manually broken down to establish a patent lumen large enough to accommodate a uterine lavage catheter. Once the catheter was placed through the cervix into the uterus, an initial sample of the uterine fluid was obtained and submitted for microbiological identification and antimicrobial susceptibility testing. A solution of 0.05% povidone-iodine was used to lavage the uterus. Oxytocin (20 U, IM, q 6 h) was given after lavage to encourage evacuation of uterine contents. Bacteriologic culture results indicated growth of Streptococcus equi subsp zooepidemicus, and the uterus was infused daily after lavage with 3.1 g of ticarcillin disodium and clavulanate potassium. This treatment was performed daily for 7 days until the uterine effluent was clear and the uterus retained minimal or no fluid.
Prior to surgery, the mare was restrained in a set of stocks and received tetanus prophylaxis and flunixin meglumine (1.1 mg/kg [0.5 mg/lb], IV). Sedation was provided by administration of detomidine hydrochloride (0.01 mg/kg, IV) and butorphanol tartrate (0.01 mg/kg, IV). Following aseptic preparation, caudal epidural anesthesia was provided in a sterile manner by administration of 5 mL of 2% mepivacaine hydrochloride at the second intercoccygeal space. The mare's tail was wrapped in gauze and reflected toward the side. The perineum was aseptically prepared and a 2-billed modified vaginal speculum1 was placed in the vaginal vault to provide access to the cervix. Two stay sutures of 2-0 polyglactin 910a were placed on the dorsolateral aspect of the cervix adjacent to the site of the intended surgical resection. Tension was placed on the stay sutures to retract the cervix caudally and facilitate creation of the wedge-shaped defect. Long Mayo scissors were used to create a full-thickness wedge-shaped defect in the cervix, with the apex pointed cranially from the external os and extending to the internal os. The base of the wedge measured approximately 3- to 4-cm wide, with a lumen of 2 to 3 cm in diameter near the internal os.
The cervical incision site was treated daily for 14 days with topical application of a compounded ointmentb made of dexamethasone (27 mg) and oxytetracycline (3.6 g) in 151 g of lanolin or vitamin A and D ointment.2 After hospital discharge, the ointment was applied to the cervix once weekly for the next 2 weeks.
During surgery, an inadvertent penetration in the dorsal aspect of the vagina created a communication with the peritoneal cavity. This 2-cm peritoneal defect was located dorsolateral to the cervix and was repaired with 2 interrupted sutures of 0-0 polyglactin 910.a A uterine catheter was maintained for 3 days following surgery to avoid contamination of the abdominal cavity with uterine content. The mare was prescribed procaine penicillin G (22,000 U/kg [10,000 U/lb], IM, q 12 h) and gentamicin sulfate (6.6 mg/kg [3 mg/lb], IV, q 24 h) for 3 days. During this time, the mare's vital parameters were within reference limits and there were no clinical signs of illness. Results of CBC and serum biochemical analysis on the first and third days after surgery remained within reference limits. No abnormalities were observed on percutaneous ultrasonography of the abdomen. Vaginal speculum examination 3 days after surgery indicated that the defect had healed completely. Antimicrobial administration was discontinued at this time.
Long-term follow-up of 5 years was established by communication with the mare's owner and primary veterinarian. The mare had no further episodes of pyometra and no continued adverse effects related to the cervical surgery. Repeated attempts were made to obtain oocytes, but efforts to produce a live foal were unsuccessful because of the mare's poor oocyte quality. The mare was retired from broodmare use 1 year after surgery and was euthanized 5 years after surgery as a result of unrelated musculoskeletal conditions.
Five other mares with transluminal cervical adhesions and secondary pyometra were treated in a similar manner, including a 10-year-old Quarter Horse, 13-year-old warmblood, 16-year-old Quarter Horse, 22-year-old Arabian cross, and 26-year-old Quarter Horse (Table 1). All had transluminal adhesions of the cervix, and in 3 mares, the cervices were also tortuous and had diverticula. Two of the mares were embryo donors with an extensive history of cervical manipulation, but the other 3 mares had never been bred. The 3 maiden mares had vaginal discharge, 1 with an episode of acute colic later determined to be caused by severe uterine distention secondary to high-volume pyometra. Median volume of fluid removed from the initial uterine lavage was 29 L (range, 5 to 80 L), with a median of 4.8 days of lavage prior to cervical surgery (range, 3 to 7 days). Bacteriologic culture of the uterine content revealed S zooepidemicus infection in 3 mares, 2 of which had concurrent infection with Proteus vulgaris or a Pasteurella sp. In 1 mare, bacteriologic culture revealed a Bipolars sp and a Cochliobolus sp, whereas the last mare had no growth on bacteriologic culture. Intrauterine treatment with 3.1 g of ticarcillin disodium and clavulanate potassium was provided to 3 mares and was combined with 600 mg of fluconazole in 1 mare. The mean follow-up time was 999.2 days (median, 963 days; range, 149 to 1,709 days). Resolution of pyometra was obtained in 4 mares; 1 mare continued to accumulate fluid in the uterus. This mare had substantial accumulation of fluid in the uterus preoperatively, which likely resulted in stretching of the mesometrium and subsequent ventral positioning of the uterus. This mare was managed with periodic uterine lavage after surgery to prevent pyometra.
Description of clinical findings and outcome in 6 mares with pyometra caused by transluminal cervical adhesions and treated by cervical wedge resection.
| Variable | Horse 1 | Horse 2 |
|---|---|---|
| Age (y) | 23 | 22 |
| Breed | Quarter Horse | Arabian cross |
| Description of cervix | Transluminal adhesions, tortuous, diverticula | Transluminal adhesions |
| Fluid removed from uterus (L) | 8 | 10 |
| Bacteriologic culture results | Streptococcus equi subsp zooepidemicus | S zooepidemicus, Proteus vulgaris |
| Lavage (d) | 7 | 4 |
| Preoperative intrauterine treatment | Ticarcillin | No |
| Preoperative systemic treatment | No | Enrofloxacin |
| Uterine fluid reoccurrence | No | No |
| Follow-up (d) | 1,800 | 1,709 |
Discussion
The cervix provides the third and final barrier between the uterus and the external environment in the mare's reproductive tract.3 The cervix is a dynamic structure that operates under the hormonal control of the estrous cycle.4,5 During periods of estrus, cervical relaxation permits semen to move into the uterus and allows for clearance of uterine contaminants after breeding. During diestrus and pregnancy, the cervix forms a seal that protects the uterine environment from contaminants within the vaginal vault. When fully dilated during parturition, it allows for passage of a foal. If the function of the cervix is compromised, the fertility of the mare may be adversely affected.4,5
Cervical adhesions are one of the reported pathological conditions that impairs the reproductive ability of mares.5 Adhesions that prevent the cervix from opening may be transluminal or vaginal in origin. Adhesions commonly result from trauma, such as lacerations sustained during parturition, attempts to resolve a dystocia, or repeated efforts at cervical manipulation that occur as a result of intrauterine treatment, artificial insemination, or embryo transfer.6 Therefore, mares of any parity status may have cervical adhesions.
Regardless of the cause, mares with transluminal cervical adhesions are at risk for the development of pyometra as a result of mechanical impairment of uterine clearance mechanisms. Pyometra is defined as the accumulation of mucopurulent material within the uterus.7 Most mares with pyometra only have involvement of the endometrium of the uterus, but in rare instances, mares may develop metritis and clinical signs of systemic illness such as fever and endotoxemia.8 Severe uterine enlargement resulting from pyometra can result in weight loss, poor performance, and signs of colic. Regardless of the severity of the disease in the uterus, all mares with pyometra are considered as infertile when bred by conventional methods because the uterine environment cannot support the development of an embryo. Diagnosis of pyometra is determined by transrectal palpation of an enlarged nongravid uterus along with the ultrasonographic appearance of hyperechoic uterine fluid accumulation. Positive results of bacteriologic or fungal culture of the endometrium support the diagnosis.8 Treatment of pyometra consists of dilating the cervix so as to enable uterine lavage and intrauterine treatment.8 Systemic administration of oxytocin or prostaglandins and exercise after lavage may encourage expulsion of uterine contents.
In severe intraluminal cervical adhesions where patency cannot be maintained and pyometra recurs, ovariohysterectomy has been the only reported option for treatment.9–11 Although routinely performed in dogs and cats, ovariohysterectomy in mares is uncommon and more difficult and is considered an invasive procedure.12,13 Because of the pelvic location of the uterus in mares, surgical access can be challenging. In 17 clinically affected mares in 1 study,11 complications following ovariohysterectomy included death, uterine and intra-abdominal hemorrhage, septic peritonitis, colic, ileus, diarrhea, intermittent fever, jugular vein thrombosis, uterine stump necrosis and abscess formation, and incisional infection. Because of the potential for contamination of the abdomen with uterine content during surgery, uterine lavage is typically done prior to surgery.14 An obvious sequela of ovariohysterectomy is permanent sterility.
For mares with pyometra secondary to transluminal cervical adhesions in the present report, the cervical wedge resection enabled treatment of pyometra in all mares and allowed for production of foals by embryo transfer in 1 mare. The surgical technique was performed in standing mares with simple instrumentation. Compared with ovariohysterectomy, the procedure was minimally invasive, with few complications. The procedure was also economically advantageous, compared with ovariohysterectomy.
Cervical adhesions likely developed in 3 mares because of their status as embryo donors and repeated manipulation of the cervix. In these mares, the cervices were severely distorted by fibrosis and diverticula. This made the initial manual breakdown of cervical adhesions to restore patency and also the subsequent resection of the cervix more difficult. In mares with such a tortuous cervix, it can be much more difficult to identify the cervical lumen and the location of the internal os. It is important to achieve temporary patency of the cervix prior to surgery to remove the mucopurulent content of the uterus.
Inadvertent penetration of the vagina can result in communication with the abdominal cavity, as in the case of mare 1. This creates the potential for contamination of the peritoneal cavity with uterine contents. The mucopurulent content within this mare's uterus had been removed prior to surgery, and the vaginal defect was repaired surgically without associated complications. This case illustrates the importance of uterine lavage to remove accumulated fluid and intrauterine antimicrobial treatment prior to surgery.
Two mares in the present report had chronic, high-volume pyometra. These mares had considerable stretching of the mesometrium and subsequently had a more ventrally positioned uterus. Although resection of the cervix enabled uterine access for treatment of pyometra, 1 mare continued to accumulate intrauterine fluid because of the dependent location of the uterus. Owners should be informed that mares with a ventrally positioned uterus may require either intermittent uterine lavage to reduce the fluid accumulation or possibly uteropexy to imbricate the mesometrium and to correct the uterine position even if cervical patency is established.15
Postoperative management of mares with cervical wedge resection was important in maintaining cervical patency. Trauma to the cervix often initiates an inflammatory reaction exceeding those that occur in the vagina or vestibule. A fibrin scaffold is produced, and if inadequate fibrinolysis occurs, fibroblasts can migrate over the scaffold and begin neovascularization. As a result, collagen is produced and adhesions can form. Removal of the wedge-shaped defect from the cervix leaves exposed submucosal and muscular surfaces that are vulnerable to further adhesion formation. Application of the compounded ointmentb appears to help promote reepithelialization and minimize adhesion formation. Additionally, manual palpation of the defect during application of the ointment helps ensure the cervix heals in a patent position.
Mares with pyometra secondary to cervical adhesions are infertile when bred by conventional methods as a result of impairment of cervical function and chronic endometrial damage. Once a mare undergoes a cervical wedge resection, its cervix is rendered incompetent and the mare can never support a pregnancy to term. However, mares may still produce foals with assisted reproductive techniques. Mares that are unable to provide embryos by routine embryo transfer methods may still produce foals through transcutaneous or transvaginal aspiration of oocytes and intracytoplasmic sperm injection or oocyte transfer to produce viable embryos. Prior to oocyte aspiration, uterine lavage may still be necessary to decrease uterine size to facilitate manipulation of the ovaries and to reduce the potential of peritoneal contamination. Provided the mare's breed registry allows for foals to be produced with assisted reproductive techniques, the cervical wedge resection can help preserve the ability of these mares to continue to provide valuable genetic material to their breed.
Vicryl, Ethicon Inc, Somerville, NJ.
Pharmacy, Veterinary Medical Teaching Hospital, Texas A&M University, College Station, Tex.
References
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