Theriogenology 66 (2006) 560–566

www.journals.elsevierhealth.com/periodicals/the

Pathogenesis and treatment of endometritis

Abstract
Inflammatory conditions of the uterus, collectively known as endometritis, can be classified as acute, chronic, active, or
subclinical. This condition causes substantial reductions in mare fertility. To diagnose and treat mares with endometrial
inflammation, it is imperative to identify predisposing factors and challenges to the reproductive tract of the mare in a chronological
order; these factors change from those of the young maiden filly to the older, multiparous broodmare. This paper addresses
predisposing factors, diagnostic procedures and therapy strategies for different mare groups.
# 2006 Elsevier Inc. All rights reserved.

Keywords: Endometritis; Post-mating endometritis; Endometrium; Uterus; Mare

1. Introduction 2. The young mare

Endometritis is an important cause of reduced One approach to infertility in the mare is to analyze the
fertility in mares. Inflammatory conditions of the uterus predisposing factors and challenges to the reproductive
may be categorized as acute, chronic, active, sub- tract in a chronological order. These factors change from
clinical, post-partum, bacterial, fungal, viral, mating- those of the young maiden filly to the older, multiparous
induced, persistent, and others. Each of these classifica- broodmare. Young mares are usually bred for the first
tions has validity in describing the infections and time between 3 and 6 years of age. During the racing or
inflammatory insults to the uterus. When presented with performance careers of fillies, many fillies achieve a high
a mare with uterine inflammation, the use of more than level of fitness. These very fit fillies lose body fat in the
one of the above terms is usually appropriate. For the perineal area. The rectum becomes displaced more
clinician, it is crucial that clients understand the anteriorly, allowing the vulva to be pulled above the
apparently simplicity of uterine infections in mares, pelvic brim. This altered perineal conformation allows
but also the complexity of endometritis. If clients have repeated fecal contamination of the vulva and vestibule.
an appreciation of the pathogenesis of endometritis, During periods of exercise, muscular fatigue and estrus
they will understand not only the goal of prevention and contribute to perineal relaxation. Aspiration of air, fecal
treatment efforts, but also the treatment failures that material and bacteria into the vestibulum and vaginal
occur. cavity is common in performance fillies. This condition is
termed pneumovagina. The above insults to the
reproductive tract are further complicated by the frequent
* Tel.: +1 717 235 3798; fax: +1 717 227 9853. supplementation of performance fillies with altrenogest
E-mail address: jhurtgen@nandivet.com. (an oral progestin) or injectable progesterone products.

0093-691X/$ – see front matter # 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2006.04.006
 J.P. Hurtgen / Theriogenology 66 (2006) 560–566 561

Susceptibility to uterine infections is enhanced when the is very common due to the extreme difficulty that can be
reproductive tract is under the influence of progesterone encountered passing the swab through the cervical canal.
[1]. The innate resistance of young mares to bacterial Post-breeding culture of uterine swabs usually yield a
endometritis can be compromised by pneumovagina and wide range of bacteria originating from breeding or from
fecal contamination resulting in vaginitis, pneumouterus the semen.
and endometritis. The above conditions are most Clients need to be informed of the expected fertility
common in racing Thoroughbreds. Perineal conforma- and potential complications prior to breeding older
tion can also be a heritable trait [2]. The conformational maiden mares. Affected mares can usually be identified
features of a recessed anus and horizontal angling of the during reproductive examinations prior to breeding,
vulva are most commonly observed in Thoroughbreds especially when these exams are performed during the
and Quarterhorses. peak of estrus [4]. Uterine fluid may be present during
Vulvoplasty surgery, also known as a ‘‘caslick diestrus or estrus, and the cervix fails to relax and dilate
procedure,’’ can protect the reproductive tract from during estrus. When these mares are to be mated,
pneumovagina and fecal contamination. Caslick suturing clinical experience indicates that cautious but persistent
the vulva in racing Thoroughbreds and other perfor- digital dilation of the cervical canal is beneficial. The
mance horses with compromised perineal conformation use of systemic or local medications to assist in cervical
is recommended to prevent repetitive bacterial chal- dilation has been attempted, but results were incon-
lenges to the reproductive tract and improve fertility of sistent. To my knowledge, the dosage and frequency of
maiden mares their first year at stud [2]. administration of PGE compounds have not been
Performance fillies are frequently given other reported [5]. The goal of cervical dilation is not only to
medications, such as anabolic steroids. The influence assist in proper placement of semen in the uterus, but
of these medications on young mares’ resistance to also to allow the mare’s post-breeding defense
endometritis is unknown. mechanisms to expel excess semen, extender, debris
Although the fertility of young maiden mares is and bacteria from the uterus after mating. Oxytocin (5–
usually considered high, >20% of maiden mares fail to 20 IU) is frequently administered IV or IM to affected
become pregnant. The cause of reduced fertility in mares 4 h after breeding. Fertility is not compromised
maiden mares is not defined but is most likely related to by oxytocin administration after breeding and prior to
estrous behavior for live cover and limited opportunities ovulation. Repeated injections of oxytocin or uterine
for mating as mares are retired from performance after lavage may be necessary to remove uterine fluid within
the breeding season has started. Endometritis has not 2–3 d post-ovulation. Because the uterus is frequently
been identified as a substantial factor in lowered fertility ineffective in clearing bacteria from these mares,
of young maiden mares. intrauterine antibiotic infusions of the uterus in
conjunction with uterine lavage are often necessary.
3. The older maiden mare Lavage fluids may include 500 mL of physiologic
saline, lactated Ringer’s solution, or embryo transfer
The fertility of older maiden mares is frequently flush fluids. The 500 mL lavage volumes are massaged
compromised. Mares as young as 8 years, but usually throughout the uterus and are retrieved from the uterus
>12 years, may be affected. Affected mares have an by gravity flow. It may be necessary to instill and
elongated, closed, fibrous cervix during estrus. The retrieve two or three volumes of lavage fluid until the
uterus is usually normal in size but it is common for retrieved fluid is clear. Uterine lavage is usually
affected mares to accumulate varying degrees of performed 4–24 h after mating. Following uterine
echolucent fluid in the uterine lumen, based on lavage, oxytocin may again be given [6–10]. The
ultrasound evaluation of the uterus [3]. The development mare’s reproductive tract should be reevaluated 24 h
of uterine edema during estrus is usually very dramatic. later to ensure that fluid accumulation has resolved,
When these mares are mated by natural cover, fertility is signs of uterine infection are not present, and the mare
very compromised because semen is likely deposited in has ovulated. The older maiden mare’s compromised
the vagina instead of in the uterus. Older maiden mares response to mating invariably recurs at subsequent
bred by artificial insemination of fresh or frozen semen, matings. If these mares become pregnant and carry a
develop an acute inflammatory reaction; the inseminate is foal to term, the foaling process appears to be normal.
rarely bacteriologically sterile, resulting in an acute Endometrial biopsy of the older maiden mare’s
endometritis. Prior to breeding, bacteriologic cultures of uterus is characterized by mild to severe widespread
uterine swabs are negative, although swab contamination dilation of the lumens of endometrial glands and
562 J.P. Hurtgen / Theriogenology 66 (2006) 560–566

periglandular fibrosis that varies from slight to moderate Specifically, if mares have had vulvoplasty performed
in severity and scattered to widespread in distribution. after breeding, an episiotomy should be performed prior
Fibrotic and nonfibrotic endometrial gland nesting are to but as close to foaling as practical to minimize
common. Inflammation is not a salient feature in these prefoaling contamination of the vaginal vault. This
endometrial biopsies unless there is fluid accumulation or practice is particularly beneficial in thin, multiparous,
the mare has been mated. Experience suggests that older and older mares. Once foaling has occurred, the vulva
maiden mares that become pregnant have a higher should be re-sutured as soon as practical. Even in mares
pregnancy loss rate than expected. Following foaling, with normal vulvar conformation, it is very common for
some of the same complications are frequently encoun- air to be aspirated into the vagina. The clinician is
tered, such as pre- and post-mating accumulation of frequently faced with a difficult decision. Many
echolucent fluid and increased risk for post-mating practitioners intentionally delay vulvoplasty in the
endometritis, despite the substantially improved char- older post-partum mare due to increased risk of post-
acter of the cervix. Alteration of myometrial activity [11], parturient uterine artery rupture due to increased blood
vascular changes in the endometrium [12], poor pressure caused by the excitement of restraint and a
myometrial response to prostanglandin [13], or altered newborn foal [16]. This practice allows substantial
mucus production [14], may explain delayed uterine pneumovagina and bacterial contamination of the
clearance of bacteria, fluid and debris following mating. reproductive tract for 2–4 d post-partum. Young
healthy mares are usually capable of mounting adequate
4. The foaling mare resistance to these periparturient challenges, but this
resistance can be weakened or lost over time, with
Foaling provides numerous challenges to the mare’s subsequent foalings, prolonged retained placenta, or an
reproductive tract. Mares foal in a variety of environ- abnormal foaling.
ments, all of which present a substantial bacterial Retained placenta can be a substantial risk factor for
challenge. During foaling, bedding materials (e.g. acute post-partum endometritis and delayed uterine
shavings, sawdust, straw, and soil) contaminate the involution. Most normal mares pass the placenta 30–
perineum during foaling, and contusions and usually 90 min after foaling. Retained placenta is frequently
minor derangement of the reproductive tract lining defined as placental expulsion 3 h after foaling.
occur. Prior to complete passage of the placenta, it can Passage of the placenta occurs over a time continuum. It
serve as a mechanism to contaminate the vaginal cavity. is not possible to impose a specific time limit on what
Relaxation of the vulva, vagina and cervix may allow constitutes delayed placental expulsion in a specific
substantial contamination by air, debris, fecal material mare. Very rapid passage of the placenta, i.e. within 10–
and bacteria. Young healthy mares undergo involution 15 min, may also be considered abnormal. Many of
of the uterus and cervix and reduce bacterial popula- these placentae have signs of substantial placentitis or
tions within 7–12 d after foaling [15]. Uterine involu- premature placental separation. Adverse events that
tion may be delayed in foaling mares with delayed first center around foaling and uterine involution are likely
estrus or in mares that are noncyclic after foaling. to contribute to acute and chronic endometritis,
The clinician needs to appreciate that when susceptibility to uterine infection and persistent post-
challenges to the reproductive system exceed resistance mating endometritis.
mechanisms, disease is likely. Post-partum disease may During an uncomplicated foaling but more fre-
be manifest as acute endometritis, delayed or incom- quently during an aggressively assisted foaling or
plete passage of the placenta, delayed uterine involu- dystocia, the cervix may be damaged or lacerated.
tion, and reduced fertility. The periparturient challenge Cervical lacerations can range from minor to full-
to the mare may come in the form of nutritional thickness, full-length tears. Regardless, there will be
imbalance, poor body condition, episiotomy, lack of compromised tissue, potential tissue necrosis and
exercise, foaling in dirty conditions (soil, shavings or inflammation. Post-partum cervical–vaginal adhesions
sawdust), dystocia, fetal malposition, delayed placental may also develop. Furthermore, the vestibulovaginal
expulsion, etc. Transient reflux of urine into the anterior sphincter may be damaged during foaling, particularly
vagina is not unusual in the immediate post-partum dystocia. The integrity of the vulva lips, vestibulova-
mare, also resulting in delayed uterine involution and an ginal sphincter and cervix are substantial barriers to
increased risk for endometritis. uterine infection and contamination. When these
Many of the above predisposing factors can be structures are damaged, there is both increased
prevented by proper nutrition and management. microbial challenge to the reproductive tract and
 J.P. Hurtgen / Theriogenology 66 (2006) 560–566 563

increased potential for altered clearance of fluids and to mating. Uterine lavage of the uterus of post-partum
bacteria following foaling or mating. mares is commonly done between 3 and 10 d post-
Parturient insults to the reproductive tract not only partum. Although this practice may be beneficial in
allow establishment of acute endometritis, but their cases of uterine infection or delayed uterine involution,
sequelae are also commonly noted in chronic endome- the routine practice of uterine lavage of post-partum
tritis cases. Mares with chronic endometritis have mares has failed to improve fertility in mares that are
sporadic exacerbation of acute endometritis, such as progressing normally through the post-partum period
following breeding or invasive internal reproductive [23,25]. Oxytocin and prostaglandin have also been
examinations. The reproductive history, endometrial used to enhance uterine involution and reduce the
biopsy results and repeated reproductive exams during potential for post-partum endometritis, with varying
estrus and diestrus and before and after mating are degrees of success [26,27].
extremely helpful in identifying mares with chronic If a mare is to be bred during foal heat, the mare’s
endometritis. Therapy for mares with chronic endome- reproductive health should be evaluated 7–9 d after
tritis needs to be directed at identified abnormalities. foaling. It is not unusual for the first estrus following
Physical abnormalities may need to be corrected by foaling to be referred to as the 9-day foal heat. However,
vulvoplasty, cervical laceration repair [17], surgery for monitoring follicular development and ovulation in
prevention of urine pooling [18] or perineal body these mares suggests that ovulation may occur as early
transection surgery [18]. Substantial weight gain may as Day 6 and extend to 15 d after foaling. There are
be necessary in thinner mares prone to pneumovagina, indications that fertility following foal-heat breedings is
even though caslick suturing of the vulva has been done. substantially improved when ovulation occurs >10 d
Any fistulae in the sutured vulva need to be repaired. after foaling, compared to 10 d after foaling [28].
Minimum contamination techniques for breeding Delaying breeding until 10 d post-partum is com-
mares by live cover or artificial insemination of mares monly practiced. For mares that ovulate prior to 10 d
with semen extended in an appropriate extender post-partum, prostaglandin is administered to induce an
containing antibiotics should improve fertility in mares early return to the second post-partum estrus.
with chronic endometritis [19,20]. In mares with This paper will not specifically address sexually
extensive vulvar suturing, it is helpful to pass a transmitted infectious endometritis. However, follow-
specialized catheter with an attached syringe into the ing the identification of Taylorella equigenitalis in
vaginal vault and guide the pipette into and through the mares and stallions in the USA, many stallions were
cervix by manual transrectal manipulation. This treated for the presence of the organism on the penis or
technique has been used for intrauterine antibiotic were treated prophylactically. Treatment consisted of
treatment and insemination of mares. Without this thoroughly washing the penis and prepuce with a 4%
technique, it may be necessary to perform repeated chlorhexidine solution, followed by application of
episiotomies and vulvoplasties over a short interval. furacin dressing to the penis and sheath for five
consecutive days. Although this treatment was effective
5. The mated mare against the organism causing contagious equine
metritis, it allowed the proliferation of Pseudomonas
Live cover matings or artificial insemination of species and Klebsiella. Mares live-covered by these
mares during the foal heat may result in acceptable stallions had reduced fertility and frequently became
fertility. However, if involution of the uterus is delayed acutely infected with Klebsiella, Pseudomonas or
or varying amounts of fluid are present at the time of Streptococcus species [29]. Uterine infections were
foal-heat breeding, fertility is substantially reduced and probably established due to substantial inoculation of
an acute endomentritis may result [21]. However, the uterus and reproductive tract with pathogenic
methods to evaluate post-partum uterine involution in a bacteria and the prolonged post-mating inflammatory
clinical setting are poorly defined and not effective. reaction. Fresh, extended semen may also be heavily
Streptococcus equi zooepidemicus, E. coli and mixed contaminated by Pseudomonas, Klebsiella, beta-hemo-
bacteria are frequently isolated from endometrial swab lytic streptococcus, and other bacteria or viruses. A
cultures [22–24]. If uterine fluid is present during foal similar acute endometritis may follow artificial inse-
heat, mating should be delayed. Affected mares can be mination of mares. Acute endometritis cases can be
treated with prostaglandin 5 d after foal-heat ovula- reduced by more appropriate hygiene of stallions at
tion. Treated mares should return to estrus in 3–5 d, mating or prior to stallion collection. Current recom-
allowing a second estrus to improve uterine health prior mendations vary from washing and rinsing the stallion’s
564 J.P. Hurtgen / Theriogenology 66 (2006) 560–566

penis using clean water with no soap or disinfectant to myometrial contractions. The excess fluid is usually
rinsing the penis with clean water following live cover. removed within hours. In more refractory cases,
The efficacy of these two management schemes should oxytocin may be given repeatedly at intervals of
be investigated. In the case of artificial insemination, 2 h to promote removal of uterine fluids. Oxytocin
antibiotics are added to the semen extender. The probably assists in fluid removal through the cervix and
antibiotics may have a broad spectrum of bacterial by absorption of fluid by the lymphatic system. Some
sensitivity or may be specifically selected for activity mares seem refractive to exogenous oxytocin treatment;
against specific bacteria. It should be noted that if the in these mares, treatment with prostaglandin or
uterus is inoculated with a specific, pathogenic bacteria cloprostenol may be indicated [6–8,10]. At the post-
during estrus, this organism will not necessarily be the breeding evaluation, the presence of echodense uterine
organism recovered days later when acute infection is fluid or purulent vulvar discharge suggests the onset of
established [1]. This phenomenon makes the study of bacterial endometrititis. These mares may benefit from
bacterial endometritis difficult and justifies the frequent the intrauterine infusion of a broad-spectrum antibiotic
use of broad-spectrum antibiotics. such as timentin, chloromycetin, ampicillin or ceftiofur
Following mating by live cover or artificial [4,10,19,33,34]. The infusion volume may range from
insemination, an endometrial inflammatory response 60 to 250 mL, depending on uterine size. Mares that
occurs. There is an influx of PMNs, fluids, and proteins have accumulated a substantial amount of uterine fluid
into the uterus, activation of uterine-derived comple- or in cases where the uterine fluid cannot be evacuated
ment, increased myometrial contractions due to using oxytocin therapy, lavage of the uterus using one or
prostaglandin release and evacuation of excess fluid, more 500 mL volumes of saline or lactated Ringer’s
bacteria, debris, and sperm. The post-mating inflam- solution may substantially improve endometrial health.
matory response removes dead and abnormal sperm and A broad-spectrum antibiotic may be infused following
seminal plasma. The neutrophils phagocytize bacteria, lavage. However, if oxytocin is administered following
thereby assisting clearance of potential acute infection. lavage (to help assure clearance of residual fluid), the
Even though seminal plasma helps moderate the post- antibiotic infusion should be delayed for 2 h. The uterus
mating inflammatory response, excess seminal fluids should be re-evaluated 24 h after the lavage procedure
are removed by uterine contractions. These uterine or antibiotic infusion to determine the persistence of
fluids are evacuated through the cervix or picked up via uterine fluid. Additional uterine lavages or treatments
the lymphatic vessels. When the above-mentioned are frequently needed in persistent mating-induced
uterine response to mating is compromised, a persistent endometritis cases. There is a high frequency of
mating-induced endometritis can result [11,13,30–32]. persistent mating-induced endometritis in affected
Persistent mating-induced endometritis increases mares from cycle-to-cycle and even year-to-year.
with mare age, bacterial contamination during mating, Affected mares have an elevated incidence of early
and other pre-existing clinical or subclinical abnorm- embryonic death in spite of post-mating treatments. The
alities of the reproductive tract. Mares that have causes of the pregnancy losses are most likely related to
detectable fluid in the uterus during diestrus or estrus mare age, a high prevalence of periglandular fibrosis,
prior to mating are at increased risk of delayed abnormal lymphatic drainage, cervical laceration, or
clearance of fluid and bacteria following mating. If other pre-existing conditions. In spite of the mating-
the fluid is not cleared within 1–2 d and the induced inflammatory reaction, mares may need to be
inflammatory response controlled by Days 2–4 post- bred 6–48 h after initial mating if ovulation has not
ovulation, pregnancy rates are low and active endome- occurred. The interval between matings will vary due to
tritis may result [5,21]. Progesterone concentrations rise stallion fertility and mating method such as live cover,
and the cervix closes rapidly immediately after AI with fresh semen, or AI with frozen semen. Seminal
ovulation; many of the mare’s defense mechanisms plasma appears to have a protective mechanism to
are lost by 24 h after ovulation. sperm in the face of an inflammatory reaction [35]. If
Transrectal palpation and ultrasound examination of mares are re-mated, treatments for persistent mating-
the uterus should be done to determine the presence of induced endometritis will need to be repeated. Fertility
uterine fluid following mating. Uterine fluid should not does not appear to be compromised in these mares if
be present 6–12 h after mating in normal mares. mated two or three times [35,36]. Housing susceptible
Oxytocin (10–20 IU) is frequently administered IV or mares near a stallion or breeding activity may also
IM to mares that have detectable uterine fluid 12–24 h induce endogenous oxytocin release and assist in the
after mating. Oxytocin induces a rapid onset of clearance of fluid and debris from the uterus [37].
 J.P. Hurtgen / Theriogenology 66 (2006) 560–566 565

Embryo transfer is a management technique that has [5] Blanchard TL, Varner DD, Schumacher J, Love CC, Brinsko SP,
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