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Placental Characteristics of Standardbred Mares
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This study examined the placental characteristics of Standardbred mares and their relationship to breeding history. The umbilical cord length, placental weight, and distribution of the three placental vascular patterns were similar to those found in Thoroughbred mares. An opposite "implantation" side and pregnancy side at term was found to be associated with long umbilical cords and a type II vascular pattern.
1. Introduction
Post-partum examination in mares generally includes an evaluation of the fetal membranes for completeness. Complete placental expulsion is imperative for maternal health; however, a more in-depth examination of the placenta can provide additional information about the pregnancy and fetal health. When positioned with the allantoic surface outward, the distinctive branching patterns of blood vessels along the surface of the allantois are easily identified. Blood flow through the umbilical cord occurs through two arteries and a single vein.
Previously, three vascular patterns have been identified in the equine placenta [1] (Fig. 1). The most common type of vasculature pattern (type I) has been observed in up to 80% of placentas [2]. Type II is seen less frequently. Recently, anecdotal evidence suggests that an aberrant placental vascular pattern (type III) may arise in cases of early twin reduction [a].
Figure 1. Equine placental vascular patterns.
Aside from placental vasculature, evaluation of the placenta also yields important measurements that are commonly compared with "normal" data obtained from research of Thoroughbreds. Standardbreds have become a breed with significant economic impact. Little information is known about normal placental characteristics and parameters in this breed.
The objective of this study was to investigate placental characteristics and their relationships to breeding history in Standardbred mares.
2. Materials and Methods
For this study, 93 Standardbred placentas were obtained from a single Standardbred breeding farm in southern Ontario. The study mares are at pasture and then, brought into the barn to foal. The placentas were collected by barn staff immediately after foaling and placed in the freezer. Two investigators evaluated all placentas and were blinded to the breeding history, except for the dam's name.
For evaluation, each placenta was positioned with the umbilical cord in a dorsal position and the allantoic side of the placenta facing out. The placentas were arranged with the greater curvature and pregnant horn in the most distal position from the cervical star forming an "F" or "Y" shape. Both investigators evaluated each placenta, and agreement was reached on the side of "implantation" and the side that held the pregnancy to term. "Implantation" side was determined by the location of the umbilical cord attachment, and pregnancy side was determined by finding the larger "pregnant" horn of the placenta.
Umbilical cord length was measured, and the entire placenta, including amnion, was weighed. The chorionic surface of the placenta was also evaluated for any indication of disease or ovillus areas that could indicate disease or a twin. Each placental artery was followed from the umbilical cord to the termination of the vessel branches to determine the vascular pattern type. Any patterns that did not clearly follow the three general patterns were deemed a variation. Variant patterns were described, and sketches were made. Each placenta was photographed using a digital camera at distance and close range in the area around the umbilical attachment. Any variant patterns had additional photographs taken.
After all placenta evaluations were complete, the breeding histories were obtained from the breeding farm veterinarians. These histories included dam and sire names, gestation length, foal weight at birth, foal status (alive or dead) at birth and at 1 wk of age, twinning history and management, and if the mare was an embryo transfer recipient. A foaling to breeding interval was also determined when data was available. This is the time between the birth of last season's foal and the time to breeding of the foal whose placenta was used in this study.
The data were analyzed using analysis of variance (ANOVA) in SAS. Comparisons between means were made using Fisher's exact test.
3. Results
Ninety-three placentas were examined for the study. Breeding history was obtained for 84 of the mares. These mares had an average gestation length of 345 ± 8 days. Two mares had twins pinched, and three mares were embryo transfer recipients. Three foals were stillborn.
Umbilical cord length ranged from 32 to 152 cm with a mean length of 58.58 ± 17.57 cm. The foal carried in the placenta with the longest umbilical cord of 152 cm was stillborn (Fig. 2). The length of this umbilical cord is considered pathologic and is also a statistical outlier in our data set (this placenta was omitted in analysis where indicated).
Figure 2. Placenta showing a pathologically long umbilical cord (152 cm; foal stillborn). Placenta has an opposite "implantation" (umbilical cord attachment) and pregnancy side.
A total of 31 sires were bred to study mares. The number of foals per sire ranged from one to eight. The sire had no effect on umbilical cord length (p = 0.3324).
The mean foal birth weight was 53. 2 ± 5.57 kg. Birth weight was statistically related to placental weight with a modest predictability (p = 0.018; R2 = 0.16).
The distribution of placental vasculature, implantation side, and pregnancy side are shown in Table 1. Type I vascular pattern was found in 73% of placentas, type II was found in 22. 6% of placentas, and type III was found in 3.2% of placentas. Some placentas showed variations from the three previously described vascular-pattern types. These variations are described in Table 2.
Table 1. Distribution of Placentas Into Vascular Pattern Categories and Side of Implantation and Pregnancy at Term | |||||
| Implantation Side | Pregnancy Side | |||
Type | Number | Left | Right | Left | Right |
Type I | 61 | 21 | 40 | 22 | 39 |
Type VI | 7 | 4 | 3 | 4 | 3 |
Total Type I | 68 (73.1%) | 25 | 43 | 26 | 42 |
Type II | 17 | 12 | 5 | 5 | 12 |
Type VII | 4 | 4 | 0 | 0 | 4 |
Total Type II | 21 (22.6%) | 16 | 5 | 5 | 16 |
Type II | 2 | 0 | 2 | 0 | 2 |
Type VIII | 1 | 0 | 1 | 0 | 1 |
Total Type III | 3 (3.2%) | 0 | 3 | 0 | 3 |
Other | 1 (1.1%) | n/a | n/a | n/a | n/a |
Total | 93 | 41 | 51 | 31 | 61 |
One Type I placenta showed the opposite side implantation and pregnancy side at term. Twin term placentas unable to categorize. |
Table 2. Description of Vascular Pattern Variations Seen in Study Placentas | ||
| Number | Description |
Type I-var | ||
A | 1 | One vessel does entire placenta; the second does the pregnant horn and part of the body. |
B | 3 | One vessel does the pregnant horn, curvature, and half of the body; the second vessel does the non-pregnant horn and the remaining body. |
C | 3 | One vessel does the pregnant horn; the second does the non-pregnant horn, curvature, and body. |
Total | 7 | |
Type II-var | ||
A | 2 | One vessel does the entire placenta; the second vessel only does the underside of the pregnant horn and curvature with small branches into the body. |
B | 1 | One vessel does the entire placenta; the second vessel overlaps and also does the non-pregnant horn. |
C | 1 | One vessel does the entire placenta except the tip of the non-pregnant horn; the second vessel does the end of the non-pregnant horn. |
Total | 4 | |
Type III-var | ||
A | 1 | One vessel does the two horns and body; the second vessel does the curvature and part of the body. |
"Implantation" side was equally distributed between left and right (p = 0.348; Table 3). Pregnancy side at term occurred significantly more on the right side of the placenta (p = 0.002). Implantation side and pregnancy side were the same in 70 of 92 placentas and were different in the remaining 22 placentas (Fig. 3). In placentas with opposite implantation and pregnancy sides, there was a significant preference for the fetus to move from left to right (p = 0.0524).
Table 3. Distribution of Placenta Implantation and Pregnancy Side at Term (n = 92) | |||
Implantation Side | Pregnancy Side at Term |
| |
| Left | Right |
|
Left | 25 | 16 | 41 |
Right | 6 | 45 | 51 |
| 31 | 61 | 92 |
Implantation side occurs equally between left and right side (p = 0.348). Pregnancy side at term occurs significantly more frequently on the right side (p = 0.002). Given that there is opposite implantation/pregnancy side, there is preference of moving from left to right (p = 0.0524). |
Figure 3. Distribution of side of blastocyst implantation and placental pregnancy side that held fetus at term (n = 92 placentas).
These opposite implantation/pregnancy side placentas were significantly more likely to have type II vasculature (21 of 22 placentas; p = 1.45 x 10 - 19) than type I (1 of 22) or type III (0 of 22).
When evaluating other placental characteristics, type II vascular pattern was found to be associated with longer umbilical cord lengths (p = 0.0163). However, if the longest umbilical cord (152 cm) is excluded from the analysis, this relationship is no longer significant (p = 0.064). When the three vascular patterns are compared, there remains a statistical difference in umbilical cord length without the outlier between type I and type II (p = 0.02; Fig. 4).
Figure 4. Means ± SD of umbilical cord length within placental vascular pattern types (152 cm; outlier not included). Pairwise comparisons show that type II differs from type I (p = 0.02). a, b indicate statistical relationship.
Pathological umbilical cords are generally defined as >80 cm long. A binomial variable "long", indicating an umbilical cord >80 cm, was created for the data. Vascular pattern was associated with "long" pathological umbilical cords (p = 0.0044; n = 6 "long" cords). Type II placentas had significantly more "long" cords than Type I (p = 0.0023; Fig. 5).
Figure 5. "Long" umbilical cords and placental vascular pattern. Type II has significantly more "long" umbilical cords than Type I (p = 0.00247). a, b indicate statistical relationship.
Mean placental weight was 4.39 ± 0.867 kg. There was no effect of placental weight on placental vascular pattern (p = 0.56) or umbilical cord length (p > 0.05).
Pre-breeding status of the mares was defined as lactating (n = 52), maiden (n = 5), barren (n = 16), or aborted during previous gestation (n = 10). The pre-breeding status of a mare has an impact on the umbilical cord length (p = 0.0350). The maiden mares had shorter umbilical cord lengths than the lactating mares (p = 0.0169). In addition, maiden mares had lower placental weights than lactating or barren mares (p = 0.03 and p = 0.05, respectively). In lactating mares, the mean foaling-to-breeding interval was 36.25 days. Umbilical cord length was not correlated with foaling-to-breeding interval in lactating mares. There was also no effect of foaling-to-breeding interval on vascular pattern.
When history of twinning was considered, no effect of twin reduction on placental vascular pattern was found (p = 0.4622). There were two sets of term twins from the study mares. Both sets of twins were type C twins as described by Jeffcott and Whitwell [3] (Fig. 6).
Figure 6. Term placenta from type C twins.
4. Discussion
Previous studies of placental characteristics have mostly been concentrated on the Thoroughbred breed. This work has been the basis of comparison for practitioners and pathologists. In 1975, Whitwell and Jeffcott [4] reported on placentas from 145 normal Thoroughbred foalings and 10 pony foalings. This study determined that 95% of umbilical cord lengths were within the range of 36 - 83 cm and that 95% of placental weights were within a range of 4.4 - 7.7 kg. The data obtained in this study was similar with 95% of umbilical cord lengths between 29 and 87 cm; 95% of placental weights ranged from 2.7 to 6.1 kg in this study. The reason for the lower placental weights in the present study may be two-fold. First, the placentas in this study had been frozen and then thawed before examination, possibly causing fluid loss during the process. Second, Standardbreds are generally a smaller breed than Thoroughbreds, and previous studies have shown that the maternal size has an effect on placental features, including mass [5].
Consistent with previous studies on placental vascular pattern, the most commonly identified pattern was type I in this study (73.1%) [2]. Type II vascular pattern was observed in 22.6% of placentas, and type III pattern was observed in only 3.2% of placentas. The results of this study showed that left and right implantations were represented in equal numbers in Thoroughbred mares. This finding was previously reported by Whitwell [2]. Significantly more pregnancies were carried in the right uterine horn (61 of 93), and in fetuses that were carried in the opposite horn to implantation side, there was a significant preference to move from the left to right side. This is in agreement with previous reports on Thoroughbred mares [2]. The reasons for the preference in mares for pregnancies to be carried in the right uterine horn is unknown, but perhaps, it may be related to anatomy of abdominal contents.
A "crossover" or opposite "implantation" and pregnancy side at term has been identified in previous studies [2,6,7]. In this study, 22 of 93 pregnancies (23.7%) were carried in the horn opposite to the side of implantation; however, this frequency of occurrence is lower than that found in a previous study of Thoroughbred mares [2]. Nonetheless, there is no account for parity within these two study groups to allow for direct comparison.
Opposite implantation/pregnancy side placentas were also statistically related to an increased umbilical cord length. However, one exceptionally long cord (152 cm) influenced the data considerably. When this placenta was excluded from the analysis, the relationship between vascular pattern and umbilical cord length weakened (p = 0.064), although comparisons between type I and type II placentas continued to show a difference in umbilical cord length. There were significantly more long cords in the type II group of placentas. Perhaps it is not surprising that in pregnancies where a fetal crossover occurs, fetal migration some distance from the site of cord implantation would naturally require a longer cord. However, it is not clear when this crossover occurs during the pregnancy. It is also unclear if the migration occurs because the cord is longer or if the longer cord develops as a result of the fetal kinesis and eventual crossover into the opposite horn.
This study also showed a strong statistical relationship between type II vascular pattern and opposite side implantation and pregnancy. This suggests that the location of the fetus in relation to umbilical cord attachment site is somehow related to the development of placental vasculature. The mechanism by which this occurs is unknown.
Long cords are pre-disposed to cord torsion, resulting in increased risk of fetal death and abortion [8-10]. Identification of risk factors for development of pathologically long umbilical cords could reduce the number of fetal losses caused by umbilical cord torsion. If fetal crossover is associated with an increased risk of developing a pathologically long umbilical cord, then the reasons for fetal crossover need to be elucidated. Clearly, the relationships between cord length, fetal crossover, and vascular pattern require additional study.
Previous studies have indicated that the location of the initial establishment of the fetus in the uterus generally alternates between successive pregnancies, which is likely caused by the smaller size and increased tone of the previously non-gravid horn [6,7]. The limitation of these studies was the use of manual palpation during early pregnancy to determine the side of the pregnancy with no or little account for migration of the fetus later in gestation. It is important to note that none of the maiden mares in the study (n = 5) showed fetal crossover. None of the 139 maiden mares in a study by Pascoe [7] showed fetal crossover from 42 days of gestation to term. It would be beneficial to follow a group of maiden mares through successive pregnancies to determine when the first fetal crossover occurs and whether there is a pre-disposition for fetal crossover in consecutive pregnancies.
In this study, pre-breeding status had an effect on umbilical cord length but not placental vascular pattern or chance of fetal crossover. However, the low number of mares in the barren, aborted, and maiden groups made it difficult to identify any differences. No statistical association between foaling-to-breeding interval and placenta characteristics (vascular pattern, umbilical cord length, or crossover) was identified. In theory, a shorter foaling-to-breeding interval (such as breeding on the foal heat) allows insufficient time for uterine involution and could pre-dispose the fetus to crossover after initial fixation in the previously non-gravid horn. In this study, a very low number of mares were bred on the foal heat (n = 6) because of farm management practices, making statistical association of foaling-to-breeding interval and placental characteristics difficult. Interestingly, the mare bred the earliest postpartum of all the mares (day 8) had a type II placental vascular pattern and fetal crossover.
Previous reports have suggested an association between type III vascular pattern and history of twin reduction [a] [1]. In this study, no association was found between twinning and type III vascular pattern. None of the placentas with a history of twin pregnancy had a type III vascular pattern, and none of the placentas showing type III vascular pattern carried a history of twinning or twin reduction. The two pregnancies in this study with a history of manual twin reduction showed a variation of type I and a type II placental vascular pattern. In the study mares, pregnancy status was determined routinely at 13 - 14 days of gestation by ultrasonography. Computerized farm records were cross-referenced to the original handwritten records to insure accuracy and avoid inadvertent omission of a case of twin reduction. This does not account for the possibility that natural twin reduction could have occurred in these mares before the initial ultrasound examination.
From this study, we concluded that Standardbred placental characteristics are similar to those previously recorded in Thoroughbred mares. Type I vascular pattern is the most commonly identified type in Standardbred mares, and type II vascular pattern is highly associated with opposite side "implantation" and pregnancy carriage. There seems to be an association between umbilical cord length and type II vascular pattern. No association was found in this study between type III vascular pattern and history of twin reduction.
Footnotes
- Whitwell KE. Personal communication. 2003.
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