CHAPTER 6. Endometritis
OBJECTIVES
While studying the information covered in this chapter, the reader should:
■ Acquire a working understanding of the mechanisms by which normal fertile mares are able to eliminate potentially pathogenic organisms from the genital tract.
■ Understand the anatomic and physiologic deficiencies that contribute to establishment of uterine infections in the mare.
■ Understand how persistent postmating endometritis differs from chronic infectious endometritis and identify methods used to reduce the incidence of embryonic loss associated with persistent postmating endometritis.
■ Acquire a working understanding of rationales for selecting methods for treatment of genital infections in the mare.
STUDY QUESTIONS
1. Review the barriers to uterine infection in the mare.
2. Discuss potential roles for the following factors in eliminating microorganisms from the uterus of the mare:
a. Immunoglobulins
b. Neutrophil migration
c. Opsonins
d. Physical clearance mechanisms:
(1) Secretions
(2) Uterine tone and contractility
(3) Lymphatic drainage
(4) Transcervical drainage
3. Regarding mares considered susceptible to postmating endometritis, discuss how to recognize which mares might be affected and how to optimize management during estrus to enhance resolution of the postmating endometritis.
4. Regarding treatment of uterine infections in the mare, discuss the rationale for and procedures used in:
a. Local antibiotic therapy
b. Uterine lavage
c. Administration of oxytocin or prostaglandins.
d. Infusion of immunity enhancers (colostrum, plasma, or bacterial filtrates)
e. Uterine curettage
f. Hormonal therapy
5. List the most common locations for genital infections in the mare.
6. List the most common organisms associated with genital infections in the mare.
7. Discuss signs of and techniques for diagnosis of endometritis in the mare.
TERMINOLOGY FOR GENITAL INFECTIONS
Most uterine infections in the mare involve only the endometrium (endometritis). Very few endometrial infections progress into deeper uterine tissues such as the myometrium (metritis). If infection progresses this deeply into the uterine wall, it can result in perimetritis and peritonitis and lead to septicemia and laminitis. The cervix can become involved (cervicitis), as can the vagina (vaginitis), usually as an extension of endometritis. Fortunately, infection of the oviducts (salpingitis) is rare because of the tight uterotubal junction in the mare. Even in the mare with a distended uterus from pyometra, the exudate rarely penetrates through the oviduct papilla to enter the oviduct.
ENDOMETRITIS
Endometritis has long been recognized as a major cause of reduced fertility in mares. Sources of uterine contamination that lead to development of endometritis include parturition, reproductive examination (even under strictly hygienic conditions), artificial insemination or natural mating, and self-contamination from conformational characteristics. Reproductively normal mares respond to uterine contamination with a transient inflammatory response that includes the activation of humoral or antibody-mediated defense mechanisms, recruitment of polymorphonuclear cells (PMNs) for bacterial phagocytosis, the release of prostaglandins, and increased uterine contractility to mechanically rid the uterus of luminal contents. These normal defense mechanisms render the reproductively normal mare resistant to persistent endometritis.
Mares that are not reproductively normal experience a breakdown in this natural defense mechanism and are considered to be susceptible to persistent endometritis. Some of the mechanisms proposed for development of persistent endometritis include insufficient opsonization of bacteria by PMNs within the uterine lumen and defective physical clearance of uterine contents. Defective physical clearance of uterine contents can result from dysfunctional uterine contractility, obstruction of physical clearance from failure of cervical relaxation, and conformational changes (e.g., pendulous uterus) that make physical removal of intrauterine contents more difficult. Persistent endometritis can be divided into two categories: persistent postmating endometritis and chronic infectious endometritis.
Persistent Postmating Endometritis
After mating or insemination, reproductively normal mares experience a transient inflammatory reaction within the uterus (in response to the presence of bacteria and sperm), which is quickly resolved (i.e., within 24 to 48 hours). This efficient clearance of the uterus after mating provides ample time for the intrauterine environment to return to normal, thus allowing for embryonic survival when the embryo enters the uterus 5 to 6 days after ovulation. In contrast, mares in which postmating endometritis fails to resolve within 48 to 72 hours are considered to have a persistent postmating endometritis. In a field fertility study that included more than 700 mare cycles, Zent et al. (1998) reported that 14% of Thoroughbred mares developed a persistent postmating endometritis. They noted that mares that accumulated a large amount of fluid after breeding tended to have lower pregnancy rates.
Management of Mares Susceptible to Persistent Postmating Endometritis
The key to enhancing fertility of mares susceptible to persistent postmating endometritis is to identify the mares before breeding and then to manage them in a manner to aid physical clearance of uterine contaminants during and immediately after the estrus of breeding. In general, mares susceptible to persistent postmating endometritis are pluriparous and older in age. However, older maiden mares may also be predisposed to this problem because of a tight cervix that fails to adequately relax during estrus, leading to retention of semen, bacteria, and inflammatory byproducts within the uterus. The result is a sustained inflammatory response that renders the environment incompatible with establishment of pregnancy.
Reproductively normal mares may accumulate a small volume of fluid within the uterus during estrus. Ultrasound examination of normal mares during estrus reveals evidence of edema within the endometrium with no fluid, or less than 1 to 2 cm in height of anechoic fluid within the lumen of the uterine horns or uterine body. One can often visualize the uterus contracting and moving fluid toward the cervix in such mares during transrectal ultrasonographic examination. In contrast, most mares that are susceptible to persistent postmating endometritis tend to accumulate larger than normal volumes of fluid within the uterus during estrus (>2 cm in luminal distention), and fluid may become hyperechoic in nature. These mares have been hypothesized to have deficient lymphatic drainage of endometrial edema, resulting in dramatic endometrial edema patterns when viewed using ultrasound. Poor uterine contractility not only impairs the lymphatic drainage but also results in failure of the uterus to evacuate contaminants. Note that uterine fluid during estrus is probably sterile unless the uterus has been contaminated. The contamination that results from breeding leads to infectious endometritis in the mare whose uterus fails to clear the bacterial contaminants. Texas workers have shown that the presence of estral uterine fluid more than 2 cm in height on ultrasound scans is a very good indicator of susceptibility to mating-induced endometritis, which allows practitioners to identify susceptible mares before breeding.
Prudent management of the mare susceptible to persistent postmating endometritis includes routine ultrasound examination during the estrus before insemination and treatment as needed with uterine ecbolics (i.e., oxytocin or prostaglandins) to stimulate uterine contractility and expel uterine contents. Uterine lavage before breeding may be indicated in those mares in which systemic treatment with ecbolics is unsuccessful in controlling intrauterine fluid accumulation. Lactated Ringer’s solution has been shown to be a safe medium for uterine lavage immediately before breeding so long as most of the fluid is evacuated during the lavage procedure.
Minimizing uterine contamination and inflammation is also important. Problems encountered during breeding that contribute to increased contamination of the uterus include excessive trauma to the genital tract, improper hygiene during breeding, excessive breeding, and a large bacterial inoculant in the stallion ejaculate. Iatrogenic contamination during artificial insemination or during examination and treatment of the genital tract can also contribute to an overwhelming inoculum. A nonsterile reusable vaginal speculum used for vaginal or cervical examination is a common culprit. Insemination should be performed under strict hygienic conditions, and semen should first be mixed with a suitable extender that contains broad-spectrum antibiotics to control bacterial growth. Ideally, breeding should be done only once within 24 to 48 hours before ovulation. Mares that must be bred by natural service may benefit from infusion of 30 to 50 mL of prewarmed antibiotic-containing semen extender into the uterus immediately before mating.
Intrauterine infusion of antibiotics after breeding is a common practice in Thoroughbred mares. However, studies evaluating the efficacy of routine postbreeding antibiotic infusions are limited, and most of the published data indicate that either the practice is either of no benefit in improving pregnancy rates or that it can in fact be detrimental. Infusion of an antibiotic solution into the uterus of a mare may be counterproductive if the solution remains retained within the uterus.
Postbreeding uterine lavage as early as 4 hours after insemination/mating aids in removal of uterine contents yet apparently does not interfere with sperm colonization of the oviducts. Therefore, we believe the safest practice is for uterine lavage or infusion to be accompanied by the use of ecbolics to promote clearance of the fluid from the uterus.
Unfortunately, the ideal interval for ecbolic administration after the uterus is infused remains unstudied. The practitioner is faced with the knowledge that administration of an ecbolic too soon after infusion could result in expulsion of the antibiotic before it may exert its beneficial effects on resident bacteria. When endometrial concentrations of various antimicrobials infused into the uterine lumen of cows and mares were evaluated, results suggested relatively rapid penetration of the few drugs studied. Therefore, until further research is done, we offer the following recommendations:
1. If uterine lavage results in complete evacuation of uterine contents, antimicrobial infusion can immediately follow the lavage. If ecbolic administration is desired, the ecbolic can be administered 4 to 8 hours later. Hopefully, this allows sufficient time for beneficial effects of the antimicrobial drug to be exerted before being expelled from the uterus.
2. If uterine lavage is accompanied or followed immediately by ecbolic administration, sufficient time should be allowed for uterine contractility to diminish before the antimicrobial infusion. Because oxytocin administered intravenously commonly results in increased uterine contractility for 20 to 50 minutes, the antimicrobial infusion could be performed as soon as 1 hour after lavage and ecbolic administration. Because the prostaglandin analog cloprostenol has been reported to result in 2 to 4 hours of sustained uterine contractions, antimicrobial infusion should be delayed by at least this interval of time.
3. If oxytocin is administered intravenously immediately before uterine lavage and if uterine lavage requires 20 to 30 minutes to complete, the antimicrobial could be infused immediately after lavage when uterine contractility from oxytocin administration should be diminishing.
Mares susceptible to persistent endometritis should be reevaluated daily after breeding via transrectal ultrasound examination until ovulation is confirmed. Uterine lavage and treatment with ecbolics may be indicated daily (or perhaps twice daily) to rid the uterus of fluid. Oxytocin administration for ecbolic effects has been shown to be safe for 2 or perhaps 3 days after ovulation. However, research has shown that administration of prostaglandins during the early postovulatory period (0 to 3 days) lowers corpus luteum (CL) production of progesterone during the ensuing diestrus, albeit for only 6 to 7 days. Because this process may contribute to CL demise, thus causing early embryonic death, the use of prostaglandins for their ecbolic effect is not recommended after ovulation has occurred. The use of oxytocin and prostaglandins during estrus and after ovulation is further discussed later in this chapter.
Chronic Endometritis
Infectious agents are capable of causing disease if the mare has a defective uterine clearance mechanism or the reproductive system is overwhelmed by a large or repeated inoculum. A common underlying problem associated with genital infection in the mare is pneumovagina, which can lead to pneumouterus. The presence of these conditions implies aspiration of air and debris into the genital tract. When these conditions exist, one or more of the three physical barriers to contamination of the uterus has been disrupted: the vulvar seal, the vestibulovaginal sphincter, or the cervix. Continuing insult, coupled with the inability to overcome infection, results in chronic endometritis. Long-standing, more severe disease shows significant infiltration of the endometrium with lymphocytes and plasma cells, confirming the chronicity of the infection. Plasmacytic infiltration implies the continuing presence of antigen, and therefore, the prognosis is guarded.
Causes of Infectious Endometritis
Numerous agents of infectious endometritis in the mare have been identified and include bacteria (both aerobic and anaerobic), fungi, and yeasts. The role of mycoplasmas, chlamydiae, and viruses is thought to be relatively insignificant, but few studies have focused on identifying these organisms as the cause of genital infections in the mare.
Diagnosis of Endometritis
Treatment of genital infections in the mare should always be preceded by a proper diagnosis. Mares are sometimes treated empirically without first pursuing a diagnosis to justify treatment, and far too often, mares are treated based on a positive culture alone, even when no evidence of inflammation is found. To substantiate a diagnosis of endometritis, signs of inflammation (e.g., the presence of fluid in the uterus or genital discharges, particularly from the uterus) should be present. Endometritis is easily confirmed with uterine cytologic analysis or biopsy. Ideally, cytology should accompany every uterine culture. Recovery of the offending organism on culture and determination of its in vitro sensitivity to antimicrobial agents allow selection of a suitable drug for treatment. The earlier the diagnosis is made, the less likely significant damage to the endometrium will occur. For this reason, mares found to be barren during fall pregnancy rechecks should be examined and treated as soon as possible.
Criteria for genital infections are presented next, followed by guidelines for various diagnostic modalities.
External Signs of Infection
These signs are rarely seen with low-grade endometritis.
■ Matting of tail hairs from chronic discharge may be present.
■ Occasional exudate is seen at the ventral commissure of the vulva.
■ Obvious exudate is seen at the vulva with an open cervix pyometra or metritis.
Findings on Examination per Rectum
■ Fluid accumulation in the uterine lumen is indicated by an enlarged uterus. An echogenic character to the fluid often indicates the presence of purulent material. Extensive fluid accumulation in diestrus, even when it is anechoic, has also been correlated with endometritis. However, the presence of small amounts of anechoic intrauterine fluid during estrus has been documented even in the absence of endometritis. A small volume of anechoic intrauterine fluid during estrus (<2 cm of intraluminal distention) is often seen in reproductively normal mares. Excessive intrauterine fluid during estrus (>2 cm) suggests poor uterine clearance mechanisms and is associated with an increased susceptibility to persistent mating-induced endometritis.
■ Massage of the uterus or vagina per rectum may express contents through a dilated cervix or vagina as vulvar discharge.
■ A slight thickening of the uterine wall may be detected in some mares with acute endometritis, but poor tone of the uterus is not a reliable indicator of endometritis.
Findings on Vaginal Speculum Examination
Findings may include:
■ Presence of inflammation indicated by reddening or increased vascularity.
■ Presence of discharge through the cervix.
■ Presence of urine pooled in the anterior vagina.
■ Presence of debris (such as manure) in the anterior vagina.
Endometrial (Uterine) Swabbing for Culture
■ Avoid contamination of the swab. Use a guarded culture instrument (i.e., a distal occlusion should be present on the swab container that prevents exposure of the swab until it is placed within the uterus), and properly clean the hindquarters of the mare. One can pass the culture instrument through a speculum to obtain a swabbing; however, with this technique, passing the instrument through the cervix of maiden mares or mares not in estrus may be difficult.
■ Perform culture when appropriate. Culture is best done in early estrus when the cervix is relaxed and the uterus is more resistant to infection, but uterine swabs can be cultured during any stage of the cycle. However, the cervix must be dilated manually to swab the uterus during diestrus.
■ Avoid interpretive error. Isolation of bacteria alone is not evidence of endometritis. Compare the results of the culture with the presence of signs of inflammation on cytology (or particularly on biopsy) to determine the significance of results. Even when guarded uterine culture swabs are used, disagreement between culture and cytology or biopsy findings is possible. This disagreement means that positive culture results can be obtained from mares without endometritis and negative culture results can be obtained from mares with endometritis.
Bacterial Endometritis
The following four organisms (listed in decreasing order of frequency) are responsible for most confirmed cases (80%) of endometritis in the mare:
■ Streptococcus zooepidemicus
■ Escherichia coli (also Enterobacter spp.)
■ Pseudomonas aeruginosa
■ Klebsiella pneumoniae
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