Chapter 20 FETAL MONITORING IN BROODMARES
Monitoring of uteroplacental function and fetal well-being in broodmares is typically requested by owners when mares are in later stages of gestation, but it may begin anytime after pregnancy has been diagnosed. The type of monitoring undertaken varies with stage of pregnancy and client wishes, and the frequency and intensity with which mares should be monitored depend on the age, fertility, reproductive history, and present health of the mare. Although the most common causes of reproductive loss in mares can vary from region to region in the United States or among regions of the world, the overall causes of pregnancy loss can be broadly regarded as falling into infective or noninfective categories. Under these classifications, the frequency with which a given diagnosis for pregnancy loss is cited in one study may differ slightly from its reported frequency in another study, but the same conditions tend to comprise the top handful of causes in most studies. In a 1993 retrospective study1 of broodmares in Kentucky, the most common infectious condition leading to reproductive loss (defined as abortion, stillbirth, and foal death within 24 hours of birth) was placentitis. In a similar study in which aborted fetuses, stillborn foals, and placentas from premature foals from 1988 and 1989 were analyzed,2 placentitis and dystocia or birth asphyxia were the most common causes of reproductive loss, but noninfectious causes of reproductive loss exceeded the infectious causes by an approximate ratio of 2:1. In that study,2 placental disorders were slightly more common than nonplacental disorders, and umbilical cord torsion was cited as an important cause of abortion. In a 2003 retrospective study3 of abortion and neonatal death in horses in the United Kingdom, umbilical cord problems were the most frequent etiology, but placentitis was also an important cause of reproductive loss.
The most common noninfectious cause of abortion is placental insufficiency, which is most often a result of competition between twin conceptuses for available endometrial surface area or degenerative changes in the endometrium caused by age, parity, or past disease. Extensive microcotyledonary interdigitation and high cotyledonary surface density on the chorioallantoic surface, together with a functional and healthy endometrium with which to interact, are necessary for normal fetal development; conditions that influence either the maternal or fetal aspect of placentation directly influence fetal size and health.4–8
Widespread use of ultrasound in broodmare practice has led to improvement in practitioners’ capabilities for early detection and reduction of twin pregnancies, leaving placentitis as the most common cause of pregnancy loss in some practices. In the author’s practice, this effect is offset by the practice of breeding valuable broodmares into advanced age. Mares do not undergo cyclic endometrial shedding like primates, and increasing age and number of foals produced are associated with degeneration and dysfunction of endometrial glands, degeneration and occlusion of endometrial vasculature, fibrosis in the endometrial stroma, myometrial atony, and development of endometrial cysts—changes collectively referred to as endometrosis.7 As a result, pregnancy loss from uteroplacental insufficiency persists despite the low prevalence of undetected twin pregnancies. Once diagnosed, placental changes can be monitored with ultrasonographic imaging, and this information, combined with that obtained from endocrine assays and fetal biophysical profiling to monitor fetal responses, yields the most comprehensive body of information available to the practitioner at present. The commercial value of breeding horses or simply the costs a client may have expended in getting a mare bred and confirmed in foal, whatever her value, are such that attempting to preserve the pregnancy and treat a compromised fetus in utero is a feasible decision in many instances.
Mares with a high-risk pregnancy warrant fetal monitoring. Conditions considered to constitute a high-risk pregnancy include a history of abortion, prolonged pregnancy, dystocia, or other gestational problems; past delivery of a compromised foal; suboptimal endometrial function; prepartum uterine artery rupture and hemorrhage; recent episode of surgery or other physiologic stressor; present systemic illness; or inappropriately early signs of impending parturition, such as premature mammary development and lactation. In mares with any of these conditions or clinical signs, fetal monitoring is useful for evaluating uteroplacental appearance and fetal responses to the condition. Multiple methods of monitoring are available to the practitioner (Box 20-1). The most applicable methods for most practitioners are routine clinicopathologic testing, ultrasound imaging, and determination of serum hormone and fetal protein concentrations; this chapter focuses on discussion of these modalities.
Box 20-1 Modalities of Assessing Pregnancy or Fetal Well-Being
DETERMINATION OF SERUM HORMONE CONCENTRATIONS
In addition to routine laboratory tests, serum hormone concentrations may also be assayed. Hormone assays are less-sensitive indicators of fetal viability than sonographic examination, because concentrations of hormones produced by the fetus or by the placenta do not always accurately predict fetal demise or decrease promptly after death of the conceptus or fetus.9 Moreover, single-point concentrations are not altogether helpful, because hour-to-hour variation in concentrations is normal. If serum or plasma hormone concentrations are the sole basis on which fetal viability is to be determined, serial blood sampling and detection of trends or changes in mean concentrations is optimal. Once-monthly blood sampling for progesterone concentration was not useful in predicting abortion in one study of 33 pregnant mares.10
Progesterone and Progestagens
The endometrial cups arise from the invasive trophoblast layer and invade the endometrium starting at days 35 to 40. The invasive nature of the endometrial cups is associated with their abbreviated lifespan, compared with that of the noninvasive trophoblast layer, which develops into the allantochorion. Exposure of the invasive trophoblastic tissue to the endometrium incites immune attack by maternal CD4+ and CD8+ lymphocytes against paternal cell antigens on the cup cells11 and leads to regression in the cups’ size by day 70 and discontinuation of function by days 120 to 150. As the endometrial cups and secondary corpora lutea regress, native progesterone concentrations in maternal serum decrease, reaching nadir levels at 240 to 300 days. Concentrations remain low throughout most of the remainder of gestation before increasing again during the last month.12
As measured concentrations of progesterone are decreasing at approximately 150 days of gestation, those of total progestagens are increasing, in part because the progesterone elaborated by fetal and maternal adrenal glands during this time undergoes metabolism by the placenta to other metabolites.13,14 During the second half of gestation, these metabolites predominate in the mare’s serum, and progesterone per se remains low, a fact that is unique to the mare among common domestic animals. The 5α dihydroprogesterone (5αDHP) metabolite of progesterone likely subserves the actions of progesterone in maintaining myometrial quiescence during the middle and last part of gestation. Progesterone and total progestagen concentrations both increase during the last month before parturition and the rate of increase becomes more rapid during the last week prior to parturition, with normal total progestagen concentrations of <10 ng/ml increasing to ≥20 μg/ml.9 Concentrations then decrease precipitously in the hours to 1 to 2 days before parturition. Decreasing or low progestagen concentrations in the last month of gestation have been associated with abortion in mares with serious medical or surgical conditions, especially when fetal hypoxia is a consequence.9 High progestagen concentrations (>10 ng/ml) detected in the middle and later stages of gestation may be an indicator of fetal stress or placentitis, reflecting an increased rate of hypothalamus-pituitary-adrenal (HPA) axis activity and fetal maturation.15,16
Because of these physiological patterns of change in progesterone and progestagen concentrations during gestation, single-point measurements of either hormone are not necessarily helpful, and serial sampling for determination of trends or mean concentrations during a given interval is recommended.17 Practitioners must be familiar with what hormones a given endocrine assay is measuring; some tests are highly specific for progesterone (e.g., radioimmunoassay and ELISA), whereas others (competitive protein binding) reflect total progestagen concentration, and this information is crucial to interpretation of results.
Estrogens
Estrone sulfate is a product of the conceptus and is useful for assessment of fetal well-being after day 40 to 45,18,19 but plasma estrone sulfate concentrations may remain in reference range even after the fetus has died or been aborted in late-gestation mares.9,20 Therefore, assay of estrone sulfate concentration for predicting abortion or determining fetal health in mares in advanced pregnancy may be less reliable. Although high estrone sulfate concentrations do not guarantee fetal viability, low concentrations are a reliable indicator of fetal demise. Determination of estrogens in pregnant mares thus may yield supporting or helpful information, but normal concentrations are not definitive proof of fetal viability. Commercial laboratories offering equine reproductive endocrine testing include BET Reproductive Laboratories (1501 Bull Lea Road, Suite 102, Lexington, KY 40511-3036) and Antech Diagnostics (1-800-872-1001 [East] or 1-800-745-4725 [West]).
Ultrasonographic Imaging
Visual assessment constitutes an important part of the examination of any patient, and ultrasonographic imaging enables sensitive and early visual detection of many changes in compromised fetuses or the intrauterine environment. Imaging studies of the fetus and uteroplacental unit are an important component of fetal monitoring, because fetal and placental structures can be performed visually and noninvasively on a real-time basis. Ultrasonography can be highly informative regarding the growth and well-being of equine fetuses, because measurements and dimensions of fetal structures can be compared against standardized growth curves. There are positive linear associations between gestational age and certain biophysical variables, although the variability in these associations increases with gestational age.21 Imaging of the fetus and uteroplacenta facilitates early detection of disease and initiation of treatment (while the foal is in utero), which in turn enhance the likelihood of survival and chance for a favorable outcome for compromised fetuses.
Fetal ultrasonography is performed transabdominally and transrectally. After approximately 90 days, the fetus resides in the abdomen, and transabdominal imaging is the most informative. Transrectal ultrasound remains the most useful throughout pregnancy for early detection of uteroplacental thickening and placental separation in the caudal portion of the chorioallantois, the area most commonly affected with placentitis from ascending infection.22,23
Mare Preparation
Sedation should be avoided if fetal activity is being assessed, because fetal activity and cardiac rhythm will be altered and may remain altered for longer than the period of sedation lasts in the mare after administration of xylazine hydrochloride.24 Because of their association with fetal oxygen supply and health, overall activity level, frequency of gross and fine motor activity, and cardiac rate and responsiveness to musculoskeletal activity are important features of ultrasonographic examination. Warming the rubbing alcohol before application facilitates acceptance of the procedure in most mares, and most do not require restraint for transabdominal ultrasonography. Ultrasound coupling gel is irritating to skin, especially after clipping, and should be removed after the examination. Sedation of mares may be necessary for safe transrectal imaging to determine uteroplacental thickness and fluid appearance at the cervical star and caudal portion of the uterus.
Transducers
Transrectal imaging with a linear array probe operating at a frequency of 5.0 to 7.5 MHz is the best means of detecting changes in the chorioallantois in the caudal portion of the uterine body and fluids in the region of the cervical star.22 Transrectal imaging should be used in examination of mares with suspected placentitis, since the ascending route of infection from the caudal portion of the reproductive tract is most common and changes at the cervical star can be seen earliest with transrectal imaging,10 although the interval between time of entry of infection across the cervix to appearance of uteroplacental thickening or placental separation can vary.25
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