Introduction

During the last three decades, the equine breeding industry has enjoyed major advancements in reproductive efficiency, due to improvements in stallion and mare management, in addition to veterinary research and intervention. Most innovations have resulted in the development of assisted reproductive technologies, aimed at improving gamete harvesting and handling, embryonic development, and ultimately conception rates. In spite of much emphasis being placed on early embryonic life, pregnancy monitoring in the mare remains a neglected area of reproductive surveillance and, once passed 60 days pregnancy, gestational profiling of the mare is generally disregarded, unless emergency circumstances require it. Additionally, the literature offers limited information on the pathophysiology of adverse gestational conditions. Resultingly, the interpretation of unfavorable pregnancy outcomes often remains, at best, speculative.

Ultrasound technology represents the most reliable, non-invasive tool for pregnancy evaluation in the mare and a complete sonographic profile of the feto-placental unit provides a very informative basis for the assessment of fetal well-being. Fetal well-being and optimal development are suggestive of a highly functional placenta, efficient feto-maternal exchange pathways, and a sound genetic component. But in the presence a low viability fetus (i.e., stunted growth, decreased levels of activity, sustained cardiac rhythm, and frequency abnormalities), it may be challenging to identify the initial source of fetal compromise, as the three compartments (fetal, placental, and maternal) are intricately connected by a network of vascular, biochemical, and hormonal signals. Maternal medical conditions and underlying endocrine disorders may further complicate the interpretation of findings.

The need for additional diagnostic tools, elucidating some of the mechanisms compromising fetal well-being, has resulted in the application of Doppler technology to a number of feto-maternal vascular structures. A similar trend has been applied for decades to the human pregnancy, where screening for feto-maternal Doppler velocimetry parameters is carried out at set intervals throughout gestation.

Pregnancy Database

Mares at risk of a complicated pregnancy and/or delivery should have a minimum data base established, through the collection of historical, biophysical, and biochemical parameters. Medical and reproductive histories of the mare aid in determining current and recurrent gestational threats, in order to formulate a monitoring plan for that pregnancy. Evaluation of feto-placental compromise, as well as the response to treatment, commonly requires sequential examinations of the pregnant mare and assessment of several factors, including biophysical and biochemical traits. Biophysical parameters are generally obtained by means of ultrasonography and fetal electrocardiography, while hormonal profiling, mammary secretions, and fetal fluid analysis represent the biochemical parameters more frequently evaluated.

Real-time ultrasonography (US) provides a non-invasive means to assess feto-placental parameters throughout gestation. Different circumstances require US evaluation of the pregnancy in equine practice:

• Elective feto-placental evaluation of pregnant mares with histories of previous complicated gestations, in order to identify early signs of derangement in fetal growth, development, and responsiveness [1–9].
  
• Routine scanning of term mares, carried out on some breeding farms, to assess fetal presentation, aiming at implementing strategies for a safe delivery, when abnormalities are detected [7,10].
  
• Emergency feto-placental evaluation, performed when gestational complications or maternal disease are present and fetal distress/compromise may be anticipated [11–15]. Under these circumstances, clinicians are often requested to assess fetal viability and formulate a prognosis on pregnancy outcome, on the basis of findings.
  
• Twin reduction by intracardiac/intra-thoracic injection (procaine penicillin), carried out at around 4 months gestation, via ultrasound guided transabdominal puncture with a spinal needle [16]. Viability of each individual fetus should be assessed prior to reduction, in order to select the least viable co-twin to undergo procedure.
  
• Twin reduction by cranio-cervical dislocation of one fetus is performed between 60 and 120 days and requires assessment of fetal viability both prior to and after procedure [17].
  
• Fetal sexing can be carried out up to 8 to 9 months of gestation, until fetal hind limbs become engaged into the pregnant horn, preventing adequate visualization. Equine fetal gender can be determined transrectally up to 4 months gestation and then by transabdominal scanning [18–21].
  
• Some fetal congenital abnormalities may be identified during the course of routine late gestational scans

Imaging of the Equine Pregnancy

Ultrasound assessment of the feto-placental unit aims at ensuring the following conditions:

1. Adequate growth and development
   
2. Appropriate levels of activity and responsive patterns
   
3. Adequate environment

Equipment

Full investigation of feto-placental well-being requires a combination of transrectal and transabdominal techniques [15]. The quality of image obtained by transabdominal ultrasonography prior to day 100 of gestation is usually of little diagnostic value.

Linear array transducers are most commonly used for transrectal ultrasonography, due to the wide popularity among clinicians in the reproductive field, ease of transducer orientation within the narrow equine pelvis, and image interpretation.

Dedicated 5 to 8 MHz transducers or multi-frequency (6–10 MHz) probes provide adequate transrectal imaging. High frequencies (7.5–10 MHz) are required when detailed structural studies are carried out, as for cervical assessment and measurement of the combined thickness of the utero-placental unit (CTUP).

Sector and convex technologies best suit transabdominal ultrasonography. Linear technology may be employed by this route, but linear transducers are less likely to obtain good contact to the mare’s abdominal wall. Transducer frequencies ranging from 2–6 MHz are required to image the fetus up to term and 5–8 MHz to obtain detailed studies of the utero-placental unit.

Patient Preparation and Technique: Transrectal Approach

Transrectal ultrasonography should always be performed at any stage of gestation to evaluate the caudal aspect of the gravid uterus. Mares are best examined restrained in stocks to ensure safety of equipment and operator. Chemical restraint should be avoided as it tends to displace the uterus forward, away from the operator’s hand. The rectal ampulla is evacuated and the uterus palpated as far forward as it can be reached, to evaluate its content, distension, and cervical tightness and length. Gentle ballotment of the uterine body will reveal the presence of fetal parts, depending on stage of gestation, fetal presentation, and proximity of the fetus to the operator’s hand. The US transducer is then placed into the rectum as far as the operator’s arm can reach and, as it is withdrawn, palpation findings are confirmed and further investigated.

Parameters to be assessed by transrectal examination include: cervix, combined thickness of the utero-placental unit (CTUP) at the cervical pole, amnion, fetal fluids and fetal eye, bi-parietal diameter, and fetal peripheral pulses (carotid pulse) when the fetus is in anterior presentation.

Patient Preparation and Technique: Transabdominal Approach

Transabdominal evaluation of the equine pregnancy can be successfully carried out from day 100 gestation to term. In the summer months, the fine coat of some breeds will make clipping and shaving quite facultative and liberal application of alcohol and US gel allows sufficient contact for adequate US imaging. In breeds with coarser coats and in colder months, clipping will become necessary, sometimes followed by close shaving or application of hair-removing creams. The area to be prepared for scanning should be brushed and washed first to remove mud and manure soiling the hair. Alcohol may be irritating on clipped skin and mineral or vegetable oils may be a better coupling medium, when frequent scanning or prolonged periods of fetal monitoring can be anticipated. The transducer should be adequately protected, particularly if mineral oil is used. In mid to late gestation, clipping should extend from the mammary gland to the xiphoid area of the sternum ventrally and should follow two curved lateral lines outspreading to each mid abdomen, while reaching from stifle to sternum. More conservative clipping may be carried out up to mid gestation, particularly with young, primiparous mares. The boundaries of the gravid uterus within the mare’s abdomen vary depending on gestational age, parity, and uterine dynamics. Mares should be adequately restrained in stocks, in quiet and relaxed surroundings. Stocks with “split” lateral doors serve best for this purpose, as the bottom half door will protect the operator from the mare’s lower limbs. Excessive maternal anxiety may have fetal implications in terms of heart rate accelerations.

Sedation of mares subjected to US examination for fetal well-being assessment should be avoided, as administration of sedatives, though well tolerated by the gravid mare [22], will depress fetal activity, cardiac frequency [23], and reactivity. The US unit should be placed at operator’s eye level, in dim light, and close enough to maintain easy access to the keyboard. The cranio-caudal orientation of the US probe should be determined. US gel is applied over the transducer’s head and scanning will commence over the midline, from the mammary gland to the xiphoid process of the sternum, until fetal parts and fluids are encountered. Parasagittal scans are then performed to delineate the boundaries of the pregnancy within the mare’s abdomen. Transverse scans will further localize the fetus and identify the ribcage and the cardiac area; the probe head is then oriented parallel to the fetal spinal cord. Fetal presentation and position are determined. Once fetal orientation has been identified, US investigations of anatomical structure and physiological events may commence.

Adequate Growth and Development

Intrauterine growth restriction (IUGR) has been defined as a deviation from (or a reduction in) expected fetal growth and is caused by multiple adverse conditions, inhibiting fetal growth potential [24]. Foals affected by IUGR represent a high risk group because of cumulative adverse effects on intrauterine survival, delivery, and post-natal adaptation, that could affect them later in life [25,26]. The presence of multiple fetuses implies a variable degree of IUGR. Several parameters can be measured to estimate fetal size in order to identify growth trends and developmental patterns. Orbital diameters/eye volume, aortic diameter, biparietal diameter and, to a lesser extent, fetal chest and femur length have all been reported as useful indicators of fetal growth. Due to their size, the latter two parameters cannot be consistently measured in full, particularly in late gestation. The aortic diameter correlates to fetal size more efficiently than other fetal structures and reference values for different gestational ages are available in the literature [26].

Orbital Diameters/Eye Volume

The fetal eye is best assessed by transrectal ultrasonography, when the fetus is in anterior presentation. Greater detail can be obtained by this route. Several studies have demonstrated a linear correlation between orbital measurements/eye measurements/eye volume and gestational age [15,26,27]. Only in late gestation, fetal eye measurements seem to plateau [9], indicating restricted growth until foaling.

No correlation though could be established between fetal eye measurements and weight of the neonate at birth. Asymmetrical IUGR may occur in mid to advanced gestation, with the fetus experiencing relatively normal head growth, resulting from preferential circulation to vital organs (brain and heart), but its body weight and somatic organs may be seriously reduced in size. Fetal eye measurements should be taken from still sonograms of the entire orbital area, when the lens is visualized (Figure 19.1). Two perpendicular diameters are measured and their sum recorded. Several measurements are taken and the average recorded for future reference.

Eye volume is calculated as follows: eye width × eye width × eye depth [9].

Aortic Diameter

Fetal aorta can be imaged per rectum only up to mid gestation. The aortic diameter should be assessed on a longitudinal scan, close to the base of the heart, just past the aortic arch (Figure 19.2), dorsal to the trachea and its bifurcation (Figure 19.3), in close proximity to the spinal cord, within the left hemithorax (Figure 19.4). Measurements should be taken during systole and a “cine recall system” proves extremely useful in obtaining the appropriate cardiac timing, particularly when FHR frequencies are elevated. Although the two vessels both traverse the fetal chest in a cranio-caudal direction, the aorta should be distinguished from the vena cava by its echodense walls, marked pulsatile activity, and the more dorsal course within the thorax, close to the spinal cord. As many as five measurements should be obtained during the course of one examination and the average calculated.

Biparietal Diameter

The fetal head is identified by transrectal or transabdominal ultrasonography and the image is frozen when the maximal cross-sectional area of the skull is obtained [28], just above the temporo-mandibular joints (Figures 19.5, 19.6, and 19.7).

Appropriate Levels of Activity and Responsive Patterns

Fetal activity is required to promote antenatal body strength and motion, to assure successful postnatal adaptation, and represents one of the most sensitive indicators of fetal viability, in association with fetal heart rate (FHR), FHR reactivity, and fetal tone. FHR accelerations and decelerations depend on a functional central nervous system (CNS) and occur in response to environmental alterations and fetal activity.

Fetal Heart Rate (FHR) and FHR Reactivity

FHR and FHR reactivity represent the most sensitive indicators of fetal well-being. FHR reactivity indicates changes in cardiac frequency, occurring in response to different stimuli. FHR declines as gestation progresses and increases during activity in the healthy, responsive fetus.

Recordings of FHR are obtained by M-mode echocardiography. The fetal cardiac area is identified within the thorax (Figure 19.8) and multiple assessments of FHR and rhythm are made by placing the M-mode cursor over cardiac structures displaying the most dynamic range of excursion (Figure 19.9). This will help to obtain high-quality tracings, where heart rate can be easily calculated and rhythm objectively evaluated. FHR is automatically calculated by the cardiac calculation package, in-built in the US unit.

Several FHR tracings are recorded, both at rest and after activity throughout the course of the examination. Recordings during fetal activity may be quite challenging to obtain, as the fetus tends to move in and out of the angle of incidence of the M-mode cursor. FHR accelerations of 25 to 40 beats per minute (bpm) for approximately 30 seconds are usually recorded during activity. Movements without FHR accelerations may be observed and accelerations in the absence of stimuli are occasionally detected (5% incidence). Sustained tachycardia [23] or a large range of FHRs may indicate fetal distress, but could be brought on by painful maternal conditions or systemic disease. Sustained bradycardia [23,29,30], inappropriate FHR for gestational age, or lack of heart rate reactivity suggests CNS depression, probably attributable to hypoxia and may indicate impending fetal demise.

Asystole may be detected by transabdominal ultrasound in association with lack of activity. Fetal cardiac rhythm is usually regular, and cardiac arrhythmias [29] are commonly associated with a negative outcome.

Peripheral Pulses

The external carotid can be evaluated transrectally in the fetus in anterior presentation, when the head and upper neck are visualized. A distinct pulsatile activity may be observed as the external carotid artery courses over the lateral compartment of the ipsilateral guttural pouch. The dark background offered by the guttural pouches, filled with fetal fluids, provides an ideal contrast to the hyperechoic wall of the artery (Figure 19.10). The common carotid trunk can be identified by B-mode and color Doppler ultrasonography in close proximity to the fetal trachea and the jugular vein, in longitudinal and cross-sectional views of the neck (Figures 19.11, 19.12, 19.13, and 19.14). M-Mode or Doppler technology may be used to obtain pulse/spectral tracings and calculate frequency. A direct correlation of peripheral pulses and fetal heart rate has been demonstrated [31]. Assessment of peripheral pulses provides an easy and effective instrument for transrectal field evaluation of fetal well-being in late gestation, when anterior presentation prevails. The fetal thyroid can be identified on each side of the upper trachea, medial to the carotid artery (Figure 19.14).

Fetal Activity

Fetal activity and tone reflect CNS function and development, with decreased activity and declining muscular strength resulting from depressed CNS function. Activity is required to ensure satisfactory muscular development and skeletal joint function, to guarantee successful postnatal adaptation. Dormant (inactive) phases are observed at all stages of pregnancy, but are more common and prolonged in late gestation, when they can last up to 60 minutes or longer on occasion. Therefore, caution should be used in the interpretation of fetal activity, and reassessments are advisable. Lack of fetal movements has been associated with a negative outcome; however, sudden bouts of excessive activity followed by abrupt cessation have also been recorded in fetuses that subsequently died [14]. The healthy equine fetus is usually very active, displaying a whole array of major and fine-tuned movements during episodes of activity. Major fetal movements include rotation along short and long axis and horizontal or vertical whole body shifting within the uterus; sometimes a combination of few of the above may be observed during a single episode of fetal activity. The number of major fetal movements per hour tends to decrease as gestation advances, although a sudden increase in fetal activity is consistently observed 24–48 hrs prior to foaling [8]. A large range of fine-tuned movements may be observed during fetal monitoring sessions, including flexion and extension of limbs, neck and head, nostril flaring, blinking, “suckling activity” (Figure 19.15), tail wagging, etc. Rhythmical breathing movements may be observed in all fetuses in advanced gestation (from 7 months gestation), when the diaphragm and the ribcage are visualized (Figure 19.8). Nevertheless, fetal breathing is intermittent in nature and cannot be consistently evaluated. Fetal breathing implies the synchronous movement of chest wall and diaphragm. Excessive convexity of the diaphragm associated with a disproportionate chest excursion is sometimes observed in distressed fetuses.

Adequate Environment

Evaluation of fetal environment includes assessment of fetal orientation, volume and quality of fetal fluids, combined thickness and contiguity of the utero-placental unit, cervical size and echotexture, and should confirm the presence of a single fetus.

Fetal Orientation: Presentation

Abnormal presentation may cause dystocia and early detection may prevent a serious perinatal crisis, by implementation of specific delivery strategies. A study conducted on 150 light breed horse pregnancies demonstrated that up to 8 months gestation the probability of finding the fetus in anterior presentation were about 50%, in posterior presentation 25%, and in transverse presentation 25% [8]. Under normal circumstances, fetal mobility gradually decreases as gestation advances and, after 9 months gestation, rotation along the short-axis allowing changes in presentation is restricted by fetal body size and the encasing of the fetal hind limbs within the gravid uterine horn [5]. Anterior presentation is easily diagnosed by transrectal ultrasonography, when fetal head structures are identified, in particular, eye, skull, and guttural pouches. The neck of the fetus is frequently flexed, with the head resting on its ribcage (Figure 19.16). Under those circumstances, when transrectal imaging of the head is not possible, identification of the tracheal rings will help confirming anterior presentation (Figure 19.17). Transverse and posterior presentations in advanced gestation may be diagnostically challenging on transrectal examination alone, as only hooves are often visualized on US. Sometimes, segments of the umbilical cord are noticed in the caudal body of the uterus, suggesting the unlikelihood of an anterior presentation, or an abnormally long cord. Multiparous mares carrying a fetus in transverse presentation close to term frequently demonstrate an abnormally shaped abdomen, overstretched crossways. Presentation should be confirmed by a transabdominal scan, whenever a clear interpretation of transrectal findings is not possible. This is often the case in mares with a flaccid pendulous abdomen and mares that sustained ruptures of the abdominal wall or of the pre-pubic tendon in previous pregnancies.

Volume and Quality of Fetal Fluids

The equine pregnancy includes an allantoic and an amniotic compartment. Distribution of allantoic fluid is directly related to fetal dynamics and uterine tone, with no preferential area of maximal fluid depth detectable. Amniotic fluid tends to collect more frequently around the cranio-ventral half of the fetus, while the amniotic membrane is usually found in close proximity to the fetal upper body (Figure 19.18). Pathological increase of fetal fluids has been reported to occur in each compartment (hydramnion and hydroallantois) [32–35

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