Pyometra in a pluriparous Standardbred mare.

Keywords: pyometra, equine, treatment.

Primary author: Dr Rob Lofstedt.  Dept of Health Management, Atlantic Veterinary College.  Additional authors:  Dr Anna  Potter (primary clinician & corresponding author: apotter@upei.ca ) and Dr Martha Mellish, both of the section of Theriogenology, Dept of Health Management, Atlantic Veterinary College & Dr Shannon Martinson of the Department of Pathology and Microbiology, Atlantic Veterinary College. Editors: Drs Rob Lofstedt (lofstedt@upei.ca) and Allan Gunn (algunn@csu.edu.au).

A 21 year-old nulliparous Standardbred mare in a teaching herd was euthanized because of respiratory pathology, lameness and a diagnosis of pyometra. Understandably, this mare had experienced numerous per vagina examinations, uterine cultures, uterine biopsies and at least one hysteroscopy.

Early in April 2019, an enlarged, fluid-filled uterus was palpable. On transrectal ultrasonography, this fluid was partially echogenic and suspected to be pus (see figure 1). Due to its size and dependency, it was not possible to delineate the uterus. It was also not possible to palpate the ovaries. Trans-abdominal ultrasonography revealed that the uterus was highly distended and at its cranial aspect, lay adjacent to the xiphoid process. Nevertheless (and typical for mares with pyometra) the mare was bright, alert and responsive and had a normal hemogram.

The mare’s ovaries containing no luteal tissue; not an unusual finding in equine pyometra. Pyometra in mares does not necessarily develop in a progesterone dominated milieu i.e. unlike the situation in cattle, cervical closure and myometrial quiescence due to progesterone is not required for the development of pyometra. In mares it is more likely that retention of  pus within the uterus is a function of deficient myometrial activity than cervical pathology (See LeBlanc et al 1994 and Troedsson 1999), especially in older animals. Occasionally however, cervical pathology is implicated.

Figure 1. Note the accumulation of moderately echogenic pus within the uterine lumen and follicles within the ovaries. This image also serves as an excellent example of  two common ultrasonographic artifacts; reverberation and enhancement through transmission (ETT). Image Copyright: Dr Martha Mellish. mmellish@upei.ca  Image size: 862 x 947 px.

During per-vagina examination, the mare’s cervix was found to be closed tightly. Cervical patency was only established after approximately 20 minutes of digital manipulation and only then, did pus drip from the vulva lips as shown in figure 2. This suggested that cervical pathology was indeed implicated in retention of pus within the uterus, perhaps in conjunction with poor myometrial tone as discussed earlier. As seen in figure 2, a large diameter stomach tube was eventually passed through the cervix to drain the uterus. Cytology and culture were performed prior to drainage of the pus.

Figure 2. The main image shows how pus dripped from the mare’s vulva after gradual dilation of the cervical canal. The inset shows how pus was then drained from the uterus. Image Copyright: Dr Martha Mellish. mmellish@upei.ca  Image size: 1513 x 1024 px

Several days after initial drainage, the uterus was  flushed repeatedly with saline (see figure 3). Then oxytocin was administered to facilitate the expulsion of any remaining fluid. In addition, 1000 mg of prostaglandin E-1 (misoprostol) in methylcellulose was applied to the cervix and cervical canal to facilitate dilation for drainage and further treatment.

Figure 3. Serial saline flushes showing the increase in clarity with each successive flush. Copyright: Dr Anna Potter apotter@upei.ca Image size 2000 x 1215

Pending culture and sensitivity results, the uterus was lavaged daily with lactated ringers or saline solution.  Two days after the initial drainage, culture results revealed Pseudomonas aeruginosa, sensitive to gentamicin, amikacin and enrofloxacin.  Treatment was initiated with 1g of gentamicin buffered with 10ml of 8.4% sodium bicarbonate infused into the uterus after uterine lavage, every 24 hours for five days.  On the fourth day of antibiotic treatment, an additional treatment of 100ml of 90% DMSO was added into the second to last flush for three days. These treatments were followed by twice daily oxytocin treatment at appropriate intervals.

Two weeks after initial dilation of the cervix and uterine flushing, ultrasonography revealed a uterus devoid of any free fluid, multiple small follicles in both ovaries and a corpus luteum. Uterine culture at that time revealed Citrobacter koseri and Streptococcus zooepidemicus. However, approximately a month days later, the uterus had re-filled with pus and uterine culture again revealed growth of Streptococcus zooepidemicus. Six days later i.e. approximately 48 days from the initial dilation of the cervix, approximately 2.5 liters of pus was drained and treatment with saline flushes, DMSO and oxytocin treatment were re-started. On this occasion, treatment lasted for four days; the antibiotic being penicillin, not gentamicin. On day four, another uterine culture revealed growth of Citrobacter koseri.

The mare was re-examined about three and a half months after initial presentation and summer rest on pasture. At that time, three liters of pus was drained from her uterus, followed by saline lavage.

In early November, 2019, re-examination revealed that a large amount of pus had accumulated in the uterus again. The mare was then euthanized and submitted for post mortem exam. Her pus-filled uterus is shown in the inset of Figure 4.

Figure 4. The pus-filled uterus of the mare seen during postmortem examination. The appearance of pus shown here is typical for equine pyometra. Image Copyright: Dr Shannon Martinson. smartinson@upei.ca  Image size: 1500 x 911 px.

Figure 5. It is probable that the cervical lesion seen here was implicated in the development of pyometra, together with general cervical cicatrization and myometrial compromise. The cause of the lesion was unknown and could not have been caused by foaling as this was a nulliparous mare. Image Copyright: Dr Shannon Martinson. smartinson@upei.ca Image size: 2002 x 1232 px.

Bearing in mind the difficulty of cervical dilation in this case and the absence of spontaneous drainage of pus before and after treatment, cervical pathology (seen in figure 5; probably fibrosis after cervical damage) was probably important in the development of pyometra in this case.

Editor’s comments: In light of the typical recurrence and usually dismal prognosis of equine pyometra, some may be critical of the handling of this case with regard to repeated attempts at physical drainage, antibiotic and anti inflammatory treatment. Consider however, that in recent years, the use of cervical wedge resection and intra-cervical stents have provided favorable outcomes in cases of equine pyometra. This suggests that even if one presumes the presence of myometrial inadequacy, attempts to dilate the cervix both physically and hormonally (using PGE analogs) may hold merit and should be considered in some cases. Of course, wedge resection and cervical stents should be considered as well.

The bacteriology in this case also deserves comment. The significance of any of the bacteria isolated is open to question. For example, a literature search of Citrobacter koseri is devoid of examples of infertility in mares so this can be presumed to be a contaminant.  Also, Streptococcus zooepidemicus is not only a common cause of endometritis in mares, it is a common commensal and contaminant of uterine cultures as well. Also, Pseudomonas aeroginosa is commonly isolated from soil samples and it therefore likely to be present on mares at pasture. The absence or presence of bacteria in single or serial cultures in this mare is also open to discussion; bacterial cultures vary in success according to sampling or culture methods. Essentially therefore, the bacterium or bacteria responsible for pyometra in this case remains a question.

Selected references:

Aguilar, J. et al. 2006. Importance of using guarded techniques for the preparation of endometrial cytology smears in mares. Theriogenology. 66:423-430

Arnold, C.E. et al. 2015 Cervical wedge resection for treatment of pyometra secondary to transluminal cervical adhesions in six mares. J. Am Vet Med Assoc. 246: 13540-1357

Blanchard, T. et al 1981. Comparison between two techniques for endometrial swab culture and between biopsy and culture in barren mares. Theriogenology 16: 541-552

Ismaïl, R. et al 2013. Methods for recovering microorganisms from solid surfaces used in the food industry: A review of the literature. Int. J. Environ. Res. Public Health. 10:6169-6183

Katila, T, 2016 Evaluation of diagnostic methods in equine endometritis. Reproductive Biol. 16:189-196

Krohn, J. et al 2019 Use of a cervical stent for long‐term treatment of pyometra in
the mare: A report of three cases  Reprod Dom Anim. 54:1155–1159.

LeBlanc M.M. et al. 1994 Scintigraphic measurement of uterine clearance in normal mares and mares with recurrent endometritis.
Equine Vet.J. 26: 109-133

Pasolini M.V. et al. 2015 Endometritis and infertility in the mare – The challenge in equine breeding industry–A review. Open access peer-reviewed chapter.

Rötting A.K. et al 2004 Total and partial ovariohysterectomy in seven mares. British Equine Vet. J. 36:29-33

Troedsson. M.H.T. 1999 Uterine clearance and resistance to persistent endometritis in the mare. Theriogenology. 52:461-471

Cervical tears

Keywords: cervix, tear, equine, mare

Cervical tears often arise as a result of foaling, especially in maiden mares.  When the cervical integrity is sufficient to protect the uterine environment during pregnancy, cervical tears do not affect fertility. However, in many cases they do so; mares fail to conceive or conceive then experience early embryonic death.

Image size:1257 x 1320px

The mare with this cervical tear (top left) was presented after a failure to repair it surgically. This is not unusual because surgical repair of the cervix is difficult and healing is usually compromised because of its relatively poor blood supply.  The mare was infertile but her endometrial biopsy indicated that her uterus should be able to maintain pregnancy. Therefore a Shirodkar-like suture (a circumferential suture used for cervical closure in humans) was placed in this cervix and the mare was in inseminated at two successive estrous periods.  However ultrasonography failed to show pregnancy on both occasions at 14 days..

This illustration also attempts to emphasize that examination using either Polanski or tubular speculums can fail to demonstrate cervical tears.  This is especially the case during estrus when the cervix is relaxed. Even during diestrus, when cervical architecture is well defined, this author was unable to diagnose cervical tears on two occasions using speculum examination. Gloved hand examinations revealed the tears and their severity in both cases.

The equine cervical canal

Keywords: cervix, anatomy, equine

Figure 1. An interesting view of the equine cervix, photographed under water to show its anatomical intricacy.  Image size:592 x 831px

Figure 2. Another view. Image size:2807 x 4174px

It is fascinating to consider the similarity of this intricacy between species. In that regard, note the complexity of the cervix of the Cow and Pilot whale, also in LORI.

A mare's cervix is similar to its uterus and vagina in that it has both inner circular and outer longitudinal smooth muscle layers. It also contains elastic tissue. The muscle of  the cervix is supplied with sympathetic innervation but the function of that innervation is not clear. If it is continuous with the sympathetic innervation of the uterus, speculation suggests that it would have predominantly beta 2 receptors, relaxing the cervix in a sympathetically dominated state; perhaps during copulation. This could facilitate entry of the ejaculate into the uterus.

Unlike the endometrium, the cervix contains no submucosal glands. On histological examination, this feature makes it immediately evident that a cervical biopsy had been taken instead of an endometrial biopsy. Almost always, this is the result of doing a so-called "blind" biopsy where the tip of the biopsy punch is not palpated transrectally during the procedure.

Although the image above shows intricate folding of the cervical mucosa, folding of the mucosa is even more complex than it appears at this magnification. Primary folds divide into secondary and even tertiary folds at a microscopic level.

The epithelium lining the cervical canal is predominantly columnar and not surprisingly, contains goblet cells that secrete mucus for sealing the canal, This mucus also contains IgA and IgG. The mucosa is also made up of ciliated cells, the functions of which are less obvious than those of the goblet cells. Ciliated cells may be important in distributing mucus across the surface of the canal, similar to the function of ciliated cells in the endometrium.

Sampling the external cervical os (instead of the uterine lumen) as part of a breeding soundness examination is potentially misleading because the whole of the vagina, including the cervical os is contaminated with bacterial in many normal mares. In normal mares, neutrophils are also found in the external cervical os.

The equine cervix cannot be grasped, elevated and manipulated as it can in cattle. Therefore, even during the luteal phase in cycling mares when the cervix is firmer than otherwise, it may be difficult to delineate. The cervix is also difficult or impossible to delineate clearly using transrectal ultrasonography.

During the luteal phase, the cervical canal is closed but in most mares, it can easily be dilated for diagnostic procedures. When a mare is bred, the cervix remains patent for several days allowing inflammatory products (contaminated fluid, semen and cytokines) to be discharged. The canal closes as progesterone secretion increases. When pregnancy is recognized, cervical tone become remarkable, even firmer than during the luteal phase in a non-pregnant mare. At 13 or 14 days after ovulation, cervical tone often precedes uterine tone as an early indication of pregnancy.

During estrus the cervix will usually relax but in some mares, especially nulliparous (maiden) mares it can be remarkably firm; the unitiated may not even be able to discern the external cervical os. In these mares, the cervix may protrude from the cranial vagina, rather like a finger pointing caudally at the examiner and some manipulation may be required to artificially inseminate the mare. In a few cases, in multiparous mares, the cervix may be so relaxed as to gape open.  In most mares however, the state is intermediate between these two descriptions.

If one is to examine a mare for evidence of cervical tears, it is important to do so during the luteal phase. During estrus, the cervix may be so relaxed that cervical architecture is lost, making the tear difficult to see or feel during per vagina examination.

Although the cervix is tightly closed during pregnancy, it can be dilated manually with caution and patience. Subjectively, pre-treatment with intracervical prostaglandin E2 (Prepidil gel. TM.) may assist one in dilating the cervix. However, even in the absence of prostaglandin treatment, the author and others have removed fetuses from uteruses as late as five months into pregnancy. This would not be possible in cattle.

Reference: 

Katila, T. 2012. The equine cervix. Pferdeheilkunde 28: 35-38