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High risk pregnant mare
© Troedsson; licensee BioMed Central Ltd. 2007
Published: 12 December 2007
Improved diagnostic techniques and advances in the understanding of equine reproductive physiology and pathology have resulted in increased pregnancy rates in mares. In contrast, the incidence of pregnancy loss has remained fairly constant at a rate of 10–15% . Pregnancy losses during late gestation (>5 months) represent an even greater problem for the equine breeding industry. Affected mares will not only fail to produce a foal, but will often have a lower conception rate during the next breeding season.
Conditions causing high risk pregnancies
Twisted umbilical cord
Abdominal tunic rupture
Prepubic tendon rupture
Indications for examination of the fetus include early lactation, vaginal discharge, maternal systemic illness, larger than normal abdominal size, suspected twinning, overdue pregnancy and a previous poor outcome of parturition [2–5].
Transabdominal ultrasonography of the equine fetus can be performed reliably after 90 days of gestation. At this time, the uterus drops over the pelvic brim and is visible from the ventral abdomen. The assessment of fetal well being is obtained through measurement of heart rate, size, movement and tone of the fetus. The thickness of the fetal membranes, echogenicity and quantity of the allantoic and amniotic fluids, and the number of fetuses provide information to evaluate the fetus.
The fetus is visible in the inguinal area and between the mammary glands in early gestation . As pregnancy progresses the fetus is found progressively more cranial. It is necessary to apply alcohol or to clip the hair on the abdomen to obtain a diagnostic image of the fetus. In late gestation, the mare should be examined from the mammary glands to the xyphoid extending to the level of the stifles on both sides of the abdomen.
Variable gestational length, size and body type of the mare and position of the fetus will affect the choice of transducer. The highest frequency transducer that will penetrate to the desired depth should be chosen. Generally a 2.5 or 3.5 MHz transducer is required to image the fetal heart in late gestation since a depth of 30 cm is often required [5, 6]. A second higher frequency transducer (7.5–10 MHz) should be used to image the uteroplacental unit . Either a curvilinear or sector scanner is preferred because they produce a pie-shaped image that allows an increasingly larger field of view in the deeper section of the image. Sedation of the mare will affect the heart rate, tone and movement of the fetus and should be avoided if possible. The ventral abdomen of the mare should be scanned in the sagittal and transverse plane.
Aortic diameter has been shown to correlate to maternal weight and is a good indicator of fetal size during late gestation . The aorta is visualized as it exits the heart and courses dorsally in the fetus adjacent to the vertebrae. The aorta is measured at the caudal border of the heart. Normal aortic diameter obtained in 32 light breeds of mares with normal pregnancies ranged from 18.5–27 mm . A smaller than normal aortic diameter has been associated with abnormal foals with low birth weight . Fetal tone should be present. A flaccid fetus that floats in the fluids is an indication of a weak or dead fetus. The normal healthy fetus should exhibit movement during the ultrasound scan. Movement may be extension or flexion of the limbs or rotation on the fetal long axis [5, 6]. As the fetus ages, it will display more complex movements .
Evaluation of mammary secretion to assess fetal maturity
Measurement of the concentration of sodium, potassium and calcium in mammary secretions of mares before foaling can provide information about impending foaling and fetal maturity . In the late pregnant mare, the electrolytes are reflecting concentrations in serum. Between 2 and 3 days before parturition, the sodium concentrations in mammary secretion decline and the potassium concentrations rise, resulting in an inversion of the electrolyte concentrations. In addition, the calcium concentrations in mammary secretion increase within a day before parturition. Analysis of milk electrolytes in high risk pregnant mares can be helpful in providing information on fetal maturity. Occationally, an inversion of sodium and potassium milk concentrations may occur prior to fetal maturity. It is therefore important to use mammary secretion electrolyte data in conjunction with gestational length and other clinical data.
The equine placenta consists of the allantochorion, the allantoamnion, and the umbilical cord. The chorionic part of the allantochorion is attached to the endometrium through microcotyledons, which integrate the endometrium throughout the uterus with exception of a small area at the internal os of the cervix, the so-called cervical star. The allantochorion supports the fetus in utero. It provides respiratory and nutrient exchange between the mare and the fetus, and it is an endocrine active organ with hormone synthesis and metabolism of importance for maintenance and normal development of the fetus. The "free floating" allantoamnion allows the fetus to move freely within the uterus. It is not attached to the allantochorion with exception of a small area at the umbilical stalk. The only attachment between the fetus and the allantoamnion is at the umbilicus. The umbilical cord has an amniotic portion and an allantoic portion. The umbilicus contains two umbilical arteries, one umbilical vein, and the urachus. The length of the cord, and the length of the allantoic and amniotic portions can vary, but is normally 50 to 100 cm long. A cord length of >80 cm has been reported to predispose to abnormal twisting of the cord and fetal death .
Evaluation of the equine placenta is routinely performed after parturition. A thorough examination of the placenta post partum provides valuable information on disease processes or dysfunctions that could have affected the well being of an aborted fetus, or potentially cause illness in the neonatal foal. However, this examination does not aid the clinician in decisions that are aimed to prevent abortion or neonatal diseases of the foal. Evaluation of the placenta in the mare can be performed by the use of ultrasonography and endocrine tests.
Ultrasonographic evaluation of the placenta
Mares grazing endophyte-infected fescue often experience premature separation of the allantochorion, increased allantochorion weight and thickness, and retained placenta. A significant increase in uteroplacental thickness and premature separation of the allantochorion has been demonstrated on transabdominal ultrasonographic examination of endophyte-infected mares. However, the thickness was not observed until an average of 8 hours before the onset of labor .
Normal upper limits for the combined thickness of the uterus and the placenta (CTUP) during late gestation [11, 20].
151 – 270 days
271 – 300 days
301 – 330 days
Additional parameters that can be evaluated using transrectal ultrasonography include changes in the amniotic membrane and fluid character. Amniotic thickening, which occurs in some cases of placentitis, can be identified using transrectal ultrasonography. Changes in allantoic and amniotic fluid character can also be identified using transrectal ultrasonography. In normal mares, allantoic fluid is commonly hypoechoic with some specular material, while amniotic fluid is frequently a shade more hyperechoic (gray) than allantoic fluid [11, 14]. Marked changes in these fluid characteristics suggest placental infection or stress to the fetus.
While transrectal and transabdominal ultrasonographic examination of the placenta is useful to detect early signs of some placental pathology, it is important to keep in mind that placental changes resulting in periparturian problems can be subtle and may not readily be detected on ultrasonographic examination. For example, a correlation between both endometrial fibrosis and angiosis, and poor chorionic villous development has been reported [22, 23]. These changes can of course not be evaluated by the use of ultrasonography, but would require other techniques.
Endocrine monitoring of the placenta
The equine placenta is part of an endocrine fetal-placental interaction, which synthesizes and metabolizes progestagens  This endocrine function of the placenta is important for maintenance of pregnancy after the endometrial cups and the secondary corpora lutea disappear around day 120 – 150 of gestation. Fetal-placental progesterone is rapidly metabolized to 5α-pregnanes. Mares with placental pathology may have increased plasma concentrations of progestagens as a result of stress to the fetal placental unit . Unfortunately, 5α-pregnanes are not readily assayed in a commercial setting, so diagnosis of placental disease using 5α-pregnane concentrations is not possible. There is cross-reactivity between 5α-pregnanes and progesterone using some commercial radioimmunoassays for progesterone. In recent studies [26, 27] using an experimental model to induce placentitis, it was found that mares that develop a chronic form of placentitis responded with increased plasma progesterone concentrations. Conversely, mares that developed acute placentitis and abortion soon after infection experienced a rapid drop in plasma progesterone concentrations. It was suggested that measurement of repeated samples of plasma progestin concentrations in mares with placentitis might be a useful method to identify mares that may abort or deliver prematurely . Furthermore, sensitivity of progesterone assays can be improved when combined with evidence of placental thickening as detected using transrectal ultrasonography .
Relaxin is produced by the equine placenta, and can be detected in peripheral blood plasma from day 80 of gestation and throughout the pregnancy . The role of relaxin during pregnancy is not fully understood, but there is some evidence that placental relaxin production is compromised in mares at risk of aborting their fetuses [31, 32]. Ryan and co-workers observed subnormal plasma relaxin concentrations in mares with abnormal pregnancies . Mares with clinical signs of placentitis and mares exhibiting signs of fescue toxicosis had suppressed plasma relaxin concentrations. There is currently no commercial test available for equine relaxin, and more research need to be performed to evaluate the usefulness of plasma relaxin as a clinical tool to diagnose placentitis and to monitor the efficacy of treatment strategies.
Management and treatment of high risk mares
High risk pregnant mares should be monitored for fetal and placental well-being. Progestin therapy is currently being implemented in humans to halt preterm labor. Presumably, the anti-prostaglandin effect of progestins contribute to reduced myometrial activity by interfering with upregulation of prostaglandin and oxytocin receptors . Without receptor formation, gap junction formation would be inhibited and uterine contractility prevented. Treatment with progestins has long been advocated to promote uterine quiescence in mares with uterine pathology. Daels and co-workers showed that supplementation of mares with the synthetic progestin altrenogest (0.088 mg/kg SID) was able to prevent prostaglandin-induced abortion .
A variety of tocolytic agents have been used in women with preterm labor including: magnesium sulfate, β sympathomimetic agents (ritodrine, terbutaline), prostaglandin synthesis inhibitors (indomethacin, suldinac, ibuprofen, aspirin), calcium channel blockers (nifedipine) and oxytocin antagonists (atosiban)  Tocolytic agents have not been shown to significantly prolong pregnancy or improve neonatal outcome when used alone. Historically, tocolytics prolong pregnancy for up to 48 hours during which time glucocorticoids can be administered to the mother in an effort to expedite fetal maturation. Clenbuterol, a β sympathomimetic agent, has been used in clinical equine practice. The effects of clenbuterol administration on uterine tone and maternal and fetal heart rates were examined by Card and Wood . Clenbuterol was administered intravenously (300 μg) to four pregnant mares throughout gestation until parturition. Uterine relaxation occurred within 3 minutes of drug administration and persisted up to 120 minutes. The authors concluded that clenbuterol was effective in causing uterine relaxation throughout gestation, and that the side effects were minimal and transient. A more recent study reported the effects of clenbuterol when administered to 29 mares late in gestation . These authors concluded that clenbuterol was not effective in preventing the onset of myometrial contractions in normal foaling mares at term. Treated mares in this study actually foaled earlier in the evening than untreated mares. The authors speculated that the relaxant effects of clenbuterol may have promoted cervical relaxation and subsequent parturition. Based on side effects detected when clenbuterol is administered to pregnant mares, and lack of effect for delaying normal parturition, the authors suggest that this agent has limited usefulness in horses.
Management of selected high risk pregnancy conditions
The risk of postoperative abortion in mares undergoing surgery for colic is surprisingly low, and not related to stage of gestation or type of lesion. In a retrospective study, Santschi and co-workers found that 18% of surviving mares that underwent colic surgery experienced pregnancy loss . Half of the abortions occurred long after the resolution of the disease, and may have been unrelated to the surgery or colic. Hypoxia and endotoxemia were identified as risk factors associated with death of the fetus. Abortions were associated with a PaO2 <80 mm Hg when surgery occurred during the last two months of gestation.
Uterine torsion usually presents as a mild colic during the last trimester of pregnancy. Diagnosis is based primarily on rectal palpation of the broad ligaments. When the uterus is torsed, the mare is at risk for uterine rupture. Options for correction include rolling the mare, or surgical correction. Rolling may be an alternative to surgery early in the third trimester, but should not be tried in mares close to term due to increased risk of uterine rupture. Surgical correction is the most effective treatment for uterine torsion, and was found to result in the highest survival rate of foals . Furthermore, the prognosis for mares and foals is best when uterine torsion occurs at <320 days of gestation .
Abdominal tunic and prepubic tendon rupture
Ruptures of the abdominal tunic or prepubic tendon are painful and result in varying degree of edema of the ventral abdomen. Mares with a rupture of the prepubic tendon have an abnormal position of the pelvis and mammary glands. The tuber coxae is tipped up and the tuber ischii tipped down. The mammary gland is displaced because of the loss of caudal attachment of the abdominal wall . The prognosis for mare and foal is poor in mares with a complete rupture. Stall confinement, anti-inflammatory drugs, and abdominal support should be implemented. The progression of the condition of abdominal muscle and tendon, and the fetal well-being should be monitored by ultrasonography. Parturition should be induced and attended when the fetus is ready for birth. Measurement of milk secretion electrolytes are helpful in determining when it is safe to induce parturition.
Hydrops is the accumulation of excessive fluid within the amniotic or allantoic cavity. The condition is uncommon in mares, and the prognosis for pregnancy is considered poor. Presenting signs include a history of rapid abdominal enlargement over 10–14 days after the 7th month of gestation. Mares will be depressed and uncomfortable with labored breathing, ventral edema, and possibly difficulty walking. Risk of uterine rupture, abdominal hernia, or prepubic tendon rupture are all increased. To save the mare, termination of the pregnancy is often recommended. However, sudden removal of abdominal fluid associated with termination of the pregnancy or foaling may result in blood pooling in the abdominal vasculature, leading to hypovolemic shock and death of the mare. Therefore supportive fluid therapy is needed at the time of foaling or termination of pregnancy to maintain blood pressure. If possible, fluid should be drained gradually prior to removing the fetus. A case of successful management of a mare with hydrops amnion, resulting in the birth of a live foal was recently reported from the University of Florida Veterinary Medical Center . The mare was closely monitored for integrity of the abdominal wall, degree of abdominal extension, and the abdomen was supported with a girdle-like device. The pregnancy was supported medically to prevent preterm labor, and the mare produced a live foal at a normal gestational time.
Placentitis in mares poses a significant threat to fetal and neonatal viability. Placentitis is commonly caused by bacteria ascending through the vagina. The most frequent bacterial pathogens implicated in equine placentitis are Streptococcus equi subspecies zooepidemicus, Escherichia coli, Klebsiella pneumonia, and Pseudomonas aeruginosa . While bacterial infection initiates disease, recent work from an experimental model of ascending placentitis in pony mares showed that premature delivery may occur secondary to inflammation of the chorion rather than as a consequence of fetal infection [43, 44]. It was suggested that these inflammatory processes may result in prostaglandin production (PGE2 and PGF2α) and stimulation of myometrial contractility, thus resulting in preterm delivery. However, in some chronic cases of placentitis, foals will experience accelerated fetal maturation. These foals will be delivered prematurely, but will be mature enough to survive in the extrauterine environment. In humans, it is thought that indirect stimulation of the fetal hypothalamic-pituitary-adrenal axis by pro-inflammatory cytokines is responsible for precocious fetal maturation [45, 46]. If this phenomenon is also true for equine fetuses, then delaying premature labor long enough to allow accelerated fetal maturation to occur may improve foal survival rates. To achieve this goal, it is necessary to promptly diagnose and effectively treat the disease. The most common signs of placentitis in mares are premature udder development (± streaming of milk) and vulvar discharge. Transrectal and transabdominal ultrasound, combined with endocrinological assays, provide additional tools for early diagnosing and monitoring progression of placentitis in mares. Pregnant mares with signs of placentitis should be treated with systemic broad spectrum antibiotics and anti-inflammatories. Using in vivo microdialysis to detect concentrations of commonly used drugs in allantoic fluid of pregnant pony mares, Macpherson and co-workers at the University of Florida found that penicillin (22,000 IU/kg, q 6 h), gentamicin (6.6 mg/kg, q 24 h) and trimethoprim sulfamethoxazole (30 mg/kg, BID) resulted in inhibitory concentrations (MIC) of these drugs in allantoic fluid and placental tissue [47, 48]. Preliminary experimental data and clinical observations suggest that long term therapy with a combination of antibiotics, altrenogest (regumate; 0.088 mg/kg), flunixin meglumine (1.1 mg/kg BID), and pentoxifylline (8.4 mg/kg BID) can positively impact pregnancy outcome with delivery of healthy foals in mares with placentitis .
Portions of this article are adapted from Troedsson M and Sage AM. Fetal/Placental Evaluation in the Mare. In: Ball B.A. (Ed.), Recent Advances in Equine Reproduction. Ithaca: International Veterinary Information Service http://www.ivis.org, 2001; Document No. A0203.0501.
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