REVIEW ARTICLE
GONÇALVES, Gustavo Romero [1], BRESSAN, Maria Clara [2], OLIVEIRA, Arielle Vitoria de [3], ANDREGHETTI, Letícia Obo [4], SPADA, Cecilia Aparecida [5], MELLO, Nicholas Martins de [6], OLIVEIRA, Valdinei Caetano [7], BONATO, Denis Vinicius [8]
GONÇALVES, Gustavo Romero et al. Evaluation of fetal membranes in mares postpartum: literature review. Revista Científica Multidisciplinar Núcleo do Conhecimento. Year. 09, Ed. 12, Vol. 02, pp. 12-26. December 2024. ISSN: 2448-0959, Access link: https://www.nucleodoconhecimento.com.br/veterinaria-en/fetal-membranes, DOI: 10.32749/nucleodoconhecimento.com.br/veterinaria-en/fetal-membranes
ABSTRACT
The placenta is the organ responsible for the interaction between mom and fetus throughout pregnancy. After birth, the placenta stop doing its function and, as it is subdivided into different membranes, now called fetal membranes. The objective of this review is to describe the anatomo-physiology of this organ and discuss the importance and correct way of examining fetal membranes in postpartum mares, taking into account the normal and abnormal findings that can be identified. The placenta acts as a barrier against pathogens and immune components and participates in the synthesis and transport of hormones essential for maintaining pregnancy. The evaluation of fetal membranes provides us with information regarding the health of the newborn foal, as well as the integrity of the reproductive tract of foaling mares and the possible damage that may occur postpartum. Ideally, fetal membranes should be evaluated as soon as they are completely externalized and the weight should be approximately 11% of the newborn foal’s live weight. Changes in color and increase in weight may indicate inflammation or even serious infections, making it thicker and opaque, and the blood vessels more evident and congested. Knowledge of the anatomy and functions of the placenta, together with an adequate assessment of the fetal membranes, has a crucial role in the clinical examination of the dam and foal, as well as allowing for early interventions and the necessary support for sick foals.
Keywords: Placenta, Equine reproduction, Placental degeneration, Umbilical cord, Yolk sac.
1. INTRODUCTION
The placenta is defined as an organ of great importance responsible for establishing the interaction between mother and concept, in order to provide adequate nutritional, metabolic, endocrine and vascular support for the fetus until the moment of birth, since growth and health are directly related to placental development and function (Vaala et al. 2006; Morresey 2011; Schlafer 2011). In mares, the placenta is characterized as diffuse microcotyledonous epitheliochorial and adeciduous, making a healthy placenta essential for fetal development (da Silva et al. 2024).
Therefore, the evaluation of fetal membranes, so called after the loss of contact with the maternal tissue after birth, becomes extremely important in cases of births of a sick foal, premature, undermature foals, stillbirths, as well as in those resulting from abortion episode (Wilsher et al. 2020). When done correctly and thoroughly, it can become an important diagnostic tool for obtaining valuable information in recognizing diseases and/or some changes that foals may present after birth (Vaala et al. 2006; Mcauliffe & Slovis 2008; Morresey 2011; Schlafer 2011; da Silva et al. 2024).
The objective of this review is to provide a brief anatomo-physiological description of this organ and talk about the importance and correct way of conducting the examination of fetal membranes in postpartum mares, taking into account the normal and abnormal findings that can be found.
2. EQUINE PLACENTA
The placenta consists of the junction between maternal tissue and fetal tissue, through which physiological exchanges occur (da Silva et al. 2024). In the equine species it has the following classification: adeciduate, referring to the degree of invasion of maternal tissue by fetal tissue; diffuse, due to the distribution and pattern of the chorionic villi; microcotyledonaria, by the type of contact between mother and child; and epitheliochorial, based on the number of layers of uterine tissue (Landim-Alvarenga 2006; Morresey 2011).
It is made up of the allantochorion, formed by the fusion between the allantois and the chorion, containing the allantoic fluid, composed of fetal excreta; it is also composed of the allantoamnion, a structure surrounding the fetus and containing amniotic fluid; and lastly, the umbilical cord (Robles et al. 2022). This, in turn, is most often fixed in the bifurcation region between the uterine horns. It is made up of two arteries, responsible for carrying oxygen-poor blood, a vein, responsible for transporting oxygen-rich blood to the fetus, and the urachus, a structure that connects the fetal bladder to the allantoic cavity through which urine is eliminated (Whitwell & Jeffcott 1975; Davies Morel 2003; Lu 2008; Morresey 2011).
The chorion makes up the outermost surface of the chorioallantoic membrane and is covered with well-vascularized villi. The inner surface of the allantochorion is called the allantoic portion, through which the large veins and arteries that come from the umbilical vessels can be visualized (da Silva et al. 2024). The chorionic portion is connected to the endometrium through microcotyledons, which cover a large part of the uterine surface, except in an area around the cervix called the cervical star, and are responsible for maintaining the connection between the mare and the fetus (Whitwell & Jeffcott 1975; Davies Morel 2003; Morrersey 2004; Landim-Alvarenga 2006; Morresey 2011; Schlafer 2011).
The main function of the placenta is to provide adequate integration between mother and child, capable of exchanging nutrients, gases and waste (da Silva et al. 2024). Furthermore, it acts as a barrier against pathogens and immune components, and participates in the synthesis and transport of hormones essential for the maintenance of pregnancy, including estrogens and progestins (Davies Morel 2003; Landim-Alvarenga 2006; Morresey 2011; Chavatte-Palmer; Derisoud; Robles 2022).
3. ASSESSMENT OF THE FETAL MEMBRANE
Despite the complexity of the relationship between the two, maternal-fetal circulation in horses is relatively poor, and in most cases it only has the capacity to support one fetus. Any change in circulation and/or in the chorioallantoic interface can result in fetal loss or impairment at birth (Morresey 2011; Robles et al. 2022).
The evaluation of fetal membranes provides us with valuable information regarding the health of the newborn foal, as well as the integrity of the reproductive tract of foaling mares and possible damage that may occur postpartum (Morresey 2004; Lu 2008; Wilsher et al. 2020).
The fetal membranes are usually completely expelled after 30 minutes or a maximum of 2 hours after birth; after this time, placental retention can be considered (Landim-Alvarenga 2006). The delay in its expulsion, or even the presence of a small fragment of the retained chorioallantoic membrane, is enough to cause serious damage to the mare, as well as metritis, laminitis, and may even progress to septicemia (Rossdale & Ricketts 2002; Lu 2008).
Some findings, such as failure to rupture the cervical star region, placentitis, early placental abruption, meconium staining of the fetus, changes in the umbilical cord, for example, very long or very short cords and kinks are all likely indicative of fetal distress during birth (Lu 2008).
In a study carried out by Pirrone et al., in 2014, they tried to relate some changes found during the evaluation of fetal membranes in the postpartum period (placental edema, hypoplasia of the chorion villi, increase and decrease in the weight of the placenta) in a total and 89 mares, with the birth of sick foals. These mares were divided into 2 groups, with group 1 made up of foals born healthy (n= 67), and group 2, made up of foals born sick (n= 22). Abnormalities were observed in 28.36% and 54.55% of the fetal membranes evaluated, respectively. Coming to the conclusion that in those animals that presented certain changes in the evaluation of fetal membranes, the proportion of foals born sick was significantly higher. Furthermore, they also noted that this value was higher in old and multiparous mares.
Cases of twin pregnancies and in mares with endometrial lesions, such as endometrial fibrosis in old mares or even in those with systemic diseases, are considered predisposing factors that can lead to a decrease in contact between the uterine wall and the placenta, and consequently, to abortion due to smaller exchange surface between mother and fetus (Leon A. et al. 2023; Tinel et al. 2023).
Wilsher and Allen, in 2003, verified the influence of mare age on placentation. After evaluating 84 postpartum fetal membranes from mares of different age groups, they were able to verify that in primiparous and older mares, the contact surface of the microcotyledons was considerably smaller than in young and multiparous mares. Relating this to the fact that first-born mares aged less than or equal to 16 years have a uterine epithelium that is less responsive to placental growth, while in old and multiparous mares aged between 5 and 9 years, this occurs due to changes degenerative signs of the endometrial wall resulting from other pregnancies. A fact also confirmed by Pazinato et al. (2015a) in a study in which the same relationship between age and placentation in English Thoroughbred mares was observed.
In another study by Klewitz et al. (2015), the direct influence of age on the increase in uterine vascular resistance in old mares was observed. Furthermore, they highlighted their susceptibility to developing endometrial cysts and periglandular fibrosis. This fact may be associated with a decrease in maternal-fetal contact.
Pazinato et al. (2015b) evaluated the histological changes in the fetal membranes of mares with chronic laminitis compared to other fetal membranes from healthy pregnant mares. In both studies, during the histopathological examination, they were able to verify the presence of inflammatory and degenerative lesions in some regions of the fetal membranes, such as areas with the absence of villi, congestion, hemorrhage, decreased arterial lumen due to greater thickening of the fetal wall. vessels in these mares. Furthermore, the birth weight of foals from these mares was numerically lower. The authors compared the findings from the work with the syndrome of arterial hypertension in pregnant women, which can lead to placental insufficiency and fetal growth restriction as a consequence of low placental blood flow and reduced oxygen supply to the fetus.
4. POSTPARTUM EVALUATION
For the correct examination of fetal membranes, knowledge of placental development, its function and the diseases involved is necessary (Schlafer 2011). The parts to be evaluated are basically composed of the chorionic and allantoic surface of the chorioallatoid membrane, the amniotic membrane, the umbilical cord, in addition to the characteristics of the accumulated secretions (Lu 2008).
Ideally, the evaluation should be carried out as soon as they are completely externalized, otherwise they should be kept in a suitable place and environment for later analysis. To do so, it is necessary to take them to a clean place, with good lighting, and have protective equipment (glasses, gloves and mask) for collecting biological material. Dirt must be removed with running water, and then the entire assembly is weighed. Therefore, the normal weight should be approximately 11% of the live weight of the newborn foal (Morresey 2004; Schlafer 2011).
To facilitate visualization of the entire fetal membrane, it is recommended that it be positioned in an “F” shape on a smooth and flat surface, so that the horizontal lines form the design of the uterine horns and the vertical line, the entire body of the uterus, ending in cervical star region (Wilsher et al. 2020). This, in turn, appears whitish and without the presence of villi, and even, in normal labor, it will be ruptured as it is the place through which the fetus usually exits. The pregnant uterine horn is easily identified, presenting a larger size, lighter color, with a thicker wall and the villi of the chorion appear to be shorter in size compared to the non-pregnant horn (Schlafer 2004; Landim-Alvarenga 2006; Schlafer 2011; Sivakumar et al. 2014). The uterine body makes up the largest portion of the fetal membranes and is thinner than the uterine horns (Rossdale & Ricketts 2002).
At the time of birth, the fetal membranes are expelled so that the allantoic portion faces outward, while the chorionic portion remains facing inward. The first has a smooth, shiny, whitish and translucent surface, with several branches of blood vessels from the umbilical cord, which connects it to the allantoamnion. While the second has a reddish color and a velvety appearance (Whitwell & Jeffcott 1975; Morresey 2004; Landim-Alvarenga 2006; Schlafer 2011; Sivakumar et al. 2014). The amniotic membrane has a whitish, translucent color, and the branches of blood vessels that are found there come from the allantois (Rossdale & Ricketts 2002; Schlafer 2004; Schlafer 2011).
According to Whitwell e Jeffcott (1975), the allantoic surface in horses can present three different vascular patterns, classified according to whether embryonic development occurred in the same place where it was implanted. This is indicated by the place where the umbilical cord is fixed. The first pattern is the most commonly observed, in which there is embryonic development in the same uterine horn in which it was implanted; the second is characterized by the change of location of the embryo implanted in one of the uterine horns, to the other horn, in which it has just developed; and finally, the third vascular pattern, considered abnormal, is associated with twin pregnancy, however, only one of the fetuses ends up reaching term, due to the other embryo having been removed, either manually or naturally.
The umbilical cord must be evaluated regarding its size, which can vary between 36 to 83 cm in length, thickness and number of turns, with this value not exceeding more than four or five spirals (Whitwell & Jeffcott 1975; Rossdale & Ricketts 2002; Lu 2008; Morresey 2011; Wilsher et al. 2020).
Both surfaces must be analyzed, so it is necessary to invert the sides. An easy way to do this is to introduce the arm at the rupture site of the cervical star to the bottom of the uterine body, and using a fold made manually in the chorionic portion, it can be carefully inverted so that no injuries occur (Schlafer 2011).
If it is not possible to carry out the examination immediately, the fetal membranes should be stored by placing them in a bucket of water, in a clean environment away from sunlight. Once this is done, possible changes that may occur as a result of storage must be taken into account, such as congestion of blood vessels in some regions where blood ends up accumulating due to gravity, and the chorionic portion may become darker as time goes by. Therefore, it is important to know the difference between some findings that are considered normal, whether as a result of storage, transport or even changes that may occur throughout fetal development, from those that are considered abnormal (Rossdale & Ricketts 2002; Schlafer 2004; Schlafer 2011).
5. NORMAL FINDINGS
Some findings considered normal and that can be commonly found during the routine evaluation of fetal membranes in horses, were described by Morresey (2004), Schlafer (2004) and Schlafer (2011), and are:
1) Area of placental degeneration: occurs due to repetitive trauma of the pelvic limbs against the placenta, when the conceptus is already in an advanced stage of growth. The chorioallantoic membrane appears swollen, thickened and sometimes the villi area is whitish at the site of compression.
2) Chorioallantoic vesicles: localized accumulation of fluid, found in the stroma of the allantoic portion, normally located around blood vessels.
3) Chorioallantoic pouches: bag-shaped structures, arising from the destruction of the endometrial calyces during pregnancy. They are found in the chorionic portion, close to the base of the pregnant uterine horn.
4) Hypomanes: formed from the segregation of cellular debris, lipid compounds and minerals present only within the allantoic cavity, the site of elimination of fetal excreta.
5) Areas with absence of villi: they are located in the cervical star region, in linear areas that cover the vessels of the umbilical cord, in the region adjacent to the uterine ostium of the uterine tubes and also in the places where the endometrial calyces are formed.
6) Amniotic plaques: these are focal areas of squamous metaplasia of amniotic cells spread evenly in the fetal portion of the amnion. They can also be commonly observed on the amniotic surface of the umbilical cord.
7) Edema of the fetal membranes: sometimes this finding can be considered normal, for example, when there is prolonged exposure of the membranes to water, or when in longer labor.
8) Passive congestion of blood vessels: may occur as a result of delays in evaluating fetal membranes.
9) Autolysis: due to the delay and time of exposure of the membranes to the environment, they begin to acquire a drier appearance, with a grayer color and areas of flaking.
10) Remaining yolk sac: the reason is not known, however in some cases, a remnant of the yolk sac can be found, located between the vessels of the umbilical cord. This may appear in its calcified form, or as a transparent bag with an accumulation of liquid inside.
Whitwell and Jeffcott, in 1975, evaluated 145 fetal membranes from mares with foals born healthy in order to verify the normalities and abnormalities that could be found during their examination. The authors described the presence of hypomanes and remaining yolk sac in all of them.
6. ABNORMAL FINDINGS
The most common conditions that will lead to fetal membrane abnormalities are ascending placental infections (placentitis) and early placental abruption. All of these can be caused by bacterial, viral and fungal infections, or even due to abnormalities related to the mare’s reproductive tract or the development of the conceptus (Morresey 2011).
Depending on the severity and time elapsed, placental infections can result in acute changes, such as edema, necrosis and accumulation of inflammatory exudate, or chronic changes, for example, fibrosis, thickening and necrosis of the fetal (Schlafer 2004; Schlafer 2011).
Congestion of chorioallantoic blood vessels can be caused by inflammatory processes (placentitis) and blood stasis (torsion or compression of the umbilical cord). In localized placentitis, there is engorgement of the vessels. Neovascularization occurs in those processes in which the inflammation of tissues exposed to mediators is chronic (Schlafer 2011).
The areas of early placental abruption are well defined, initially they are reddish and bright, as a result of congestion of the blood vessels, and over time they become pale and without villi. This condition is easily identified when evaluating fetal membranes due to the integrity of the chorioallantoic membrane and the absence of rupture at the cervical star site (Schlafer 2011).
The absence of part of the chorioallantoic membrane in a specific location indicates that a fragment has been retained in the uterus. If this is observed, it is essential to consider the treatment so that it is removed as soon as possible, in order to avoid the proliferation of agents that cause infections in the mare’s reproductive tract, which can lead to serious complications (Rossdale & Ricketts 2002).
The most common changes found in the umbilical cord are its thickening and congestion, which can contribute to its torsion, and consequently, restrict blood flow from the placenta to the fetus and vice versa (Wilsher et al. 2020). Very long cords help to cause torsion without it being associated with infectious causes. Along with this, distension of the urachus is observed. Shorter umbilical cords (< 30 cm) predispose them to rupture and early placental abruption (Schlafer 2004; Schlafer 2011).
In some cases, the presence of the remaining calcified yolk sac may be considered an abnormality. Rarely, due to its location and as it grows, there is the possibility of it ending up damaging the blood flow of the umbilical vessels due to compression (Schlafer 2011). Furthermore, the presence of aneurysms, intramural hematomas, vascular thrombosis and umbilical cord edema must also be considered (Schlafer 2004).
Abnormal attachment of the umbilical cord can lead to prolonged pregnancy and delayed fetal growth. This is determined by inadequate fixation of the conceptus in the uterus, or by a change in the site of development. The umbilical cord fixed in the ventral region of the uterine horn and in the body of the uterus is considered abnormal, and may or may not cause complications (Wilsher et al. 2009).
Episodes of more serious infections (bacteria and fungi) can also affect the amniotic membrane, making it thicker and opaque, and the blood vessels more evident and congested. Furthermore, in some cases, this membrane acquires a yellowish or greenish color, indicating that meconium has been released inside it (Rossdale & Ricketts 2002).
Autolysis of fetal membranes is difficult to differentiate from necrosis, depending on the time elapsed between birth and the evaluation examination. When possible, in cases where there is necrosis, there will also be signs of inflammation (Schlafer 2004).
In addition to detecting visible changes, weighing fetal membranes can help diagnose some conditions. An increase in your weight may reveal an inadequate accumulation of fluid in the fetal membranes (inflammation). Whereas, a decrease in this value is indicative of the lack of some portion of the expelled membranes, which could be considered the retention of a fragment within the uterus, or extensive areas of the chorionic portion with the absence of villi (Mcauliffe & Slovis 2008; Morresey 2011).
If the presence of any of these changes described above is evident, sending materials for more specific examinations can help in obtaining more information. The swab for cytology and culture examination, and the collection of fragments of fetal membranes for histopathology are indicated in these cases (Rossdale & Ricketts 2002). Schlafer (2004) describes a protocol for collecting materials for histopathological evaluation. The author suggests obtaining fragments from seven regions of the fetal membranes, including the body of the fetal membranes, the pregnant and non-pregnant horns, the bifurcation region between the horns, the amniotic membrane, the umbilical cord and the region of cervical star, one of the most important areas when it comes to ascending infections.
Lins et al., in 2012, evaluated the clinical and metabolic changes of 50 newborn foals, in relation to the histopathological findings of their respective placentas. These were divided into two groups, each consisting of 25 animals, with the second group representing foals with changes at birth. Once this was done, they were able to verify that the presence of degenerative and/or inflammatory lesions observed in the histopathological examination in all the fetal membranes of the weakened foals was compatible with their clinical presentation.
In another study, carried out by Bianco et al., in 2014, a histomorphometric evaluation was carried out on 14 fetal membranes from recently foaled mares, separated into two groups. Group 1 was made up of 7 fetal membranes from normal births and healthy foals, while group 2 was made up of another 7 membranes also from normal births, but foals born sick. As a result of the evaluation, an increase in the weight of four fetal membranes was noted, and a decrease in this value in two other membranes in the second group, in addition to all of these demonstrating diffuse hypoplasia of the chorion villi.
7. CONCLUSION
The adequate knowledge about the anatomy and function of the equine placenta, and its correct evaluation in the post-partum period, taking into account normal and abnormal findings, is an important part of the clinical examination of both the mother and the newborn foal, as it can provide us with valuable information for a more accurate diagnosis. Therefore, it ensures that we intervene as quickly as possible in order to provide adequate support to the so-called “foal at risk”, in addition to helping us create preventative measures if more than one mare presents the same condition.
REFERENCES
Bianco, C., Pirrone, A., Boldini, S., et al., 2014, Histomorphometric parameters and fractal complexity of the equine placenta from healthy and sick foals, Theriogenology, 82(8), 1106-1112.
Chavatte-Palmer, P., Derisoud, E., Robles, M., 2022. Pregnancy and placental development in horses: an update. Domestic Animal Endocrinology, 79, 106692.
da Silva, G. C., Nogueira, C. E. W., Corcini, C. D., Júnior, A. S. V., da Rosa Curcio, B. (2024). Avaliação histomorfométrica do corioalantóide na espécie equina com o uso da análise digital de imagens. Scire Salutis, 14(1), 24-30.
Davies Morel, M.C.G., 2003, Anatomy and physiology of Pregnancy in the mare. In: Equine reproductive physiology, breeding and stud management. 2nd ed. Cambridge: CABI Publishing, 47–67.
Klewitz, J., Struebing, C., Rohn, K., et al., 2015, Effects of age, parity, and pregnancy abnormalities on foal birth weight and uterine blood flow in the mare, Theriogenology, 83(4), 721–729.
Landim-Alvarenga, F.C., 2006, Reconhecimento materno do concepto e início da placentação. In: Prestes N.C, Landim-Alvarenga F.C., Obstetrícia Veterinária. 1st ed. Rio de Janeiro: Guanabara Koogan, 22-39.
Leon, A., Pillon, C., Tebourski, I., et al., 2023, Overview of the causes of abortion in horses, their follow-up and management, Reproduction in Domestic Animals, 58(2), 93-101.
Lins, L.A., Finger, I.S., Fernandes, C.G., et al., 2012, Resposta clínica e metabólica de potros neonatos em relação aos achados histopatológicos da placenta na égua, Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 64, 1436–1441.
Lu, K.G., 2008, Placental evaluation in horses, Proceedings of the North American Veterinary Conference, 22, Orlando, Florida, 125–126.
Mcauliffe, S.B., Slovis, N.M., 2008, Color atlas of diseases and disorders of the foal. Edinburgh: Saunders Elsevier.
Morresey, P.R., 2004, How to perform a field assessment of the equine placenta, Proceedings of the 50th Convention of the American Association of Equine Practitioners, 50, 409–414.
Morresey, P.R., 2011, The placenta. In: Mckinnon A.O., Squires E.L., Vaala W.E., et al., Equine reproduction. Oxford: Wiley-Blackwell, 84–95.
Pazinato, F.M., Curcio, B.R., Fernandes, C.G. et al., 2015a, Histological features of the placenta and their relation to the gross and obstetrical findings in Thoroughbred mares (no prelo), Reproduction in Domestic Animals.
Pazinato, F.M., Curcio, B.R., Feijó, L.S., et al., 2015b, Morfometria vascular da placenta em éguas com laminite crônica (no prelo), Placenta.
Pirrone, A., Antonelli, C., Mariella, J., et al., 2014, Gross placental morphology and foal serum biochemistry as predictors of foal health, Theriogenology, 81(9), 1293–1299.
Robles, M., Loux, S., de Mestre, A. M., Chavatte-Palmer, P., 2022. Environmental constraints and pathologies that modulate equine placental genes and development. Reproduction, 163(3), R25-R38.
Rossdale, P.D., Ricketts, S.W., 2002, Evaluation of the fetal membranes at foaling. Equine Veterinary Education, 5, 78-82.
Sivakumar, A., Kulasekar, K., Devanathan, T.G., et al., 2014, Morphometry of Equine Placenta, The Indian Journal of Animal Reproduction, 35(1), 1-4.
Schlafer, D.H., 2011, Examination of the placenta. In: Mckinnon A.O., Squires E.L., Vaala W.E., et al., Equine Reproduction. 2nd ed. Ames, Iowa: Wiley Blackwell, 99-110.
Schlafer, D.H., 2004, Postmortem examination of the equine placenta, fetus, and neonate: methods and interpretation of findings, Proceedings of American Association of Equine Practitioners, 50, 1–19.
Tinel, J. B., Veras, M. M., Waked, D., Alonso, M. A., Fernandes, C. B., 2023. Comparative stereological evaluation of the term allantochorion membrane in the mare pregnant with mule foals and equine foals. Animal Reproduction Science, 250, 107201.
Vaala, W.E., House, J.K., Madigan, J.E., et al., 2006, Conduta inicial e exame físico do neonato. In: Smith B.P., Medicina Interna de Grandes Animais. 3nd ed. Barueri: Manole, 277-293.
Whitwell, K.E., Jeffcott, L.B., 1975, Morphological studies on the fetal membranes of the normal singleton foal at term. Research in Veterinary Science, 19(1), 44–55.
Wilsher, S., Allen, W.R., 2003, The effects of maternal age and parity on placental and fetal development in the mare, Equine veterinary jornal, 35(5), 476-483.
Wilsher, S. et al., 2020. Morphological characteristics of the placenta and umbilical cord of Arabian mares foaling in The United Arab Emirates. Journal of Equine Veterinary Science, 91, 103124.
Wilsher, S., Ousey, J., Allen, W.R., 2009, Abnormal umbilical cord attachment sites in the mare: a review illustrated by three case reports, Equine veterinary jornal, 41, 930-939.
[1] Master’s Degree in Animal Science; Bachelor’s Degree in Veterinary Medicine. ORCID: https://orcid.org/0000-0003-1467-1406. Currículo Lattes: http://lattes.cnpq.br/6977651873179536.
[2] Degree in Veterinary Medicine. ORCID: https://orcid.org/0009-0006-1481-3477.
[3] High school completed. ORCID: https://orcid.org/0009-0001-0146-5470.
[4] Degree in Veterinary Medicine. ORCID: https://orcid.org/0009-0008-7554-7162.
[5] Master’s Degree in Agronomy; Degree in Veterinary Medicine. ORCID: https://orcid.org/0009-0004-3807-9196.
[6] Master’s Degree in Animal Science; Bachelor’s Degree in Veterinary Medicine. ORCID: https://orcid.org/0009-0000-0820-1913.
[7] Degree in Veterinary Medicine. ORCID: https://orcid.org/0009-0009-1193-0661.
[8] Degree in Veterinary Medicine, Master and Doctorate in Animal Science. ORCID: https://orcid.org/0000-0001-6974-4858.
Material received: April 23, 2024.
Material approved by peers: December 4, 2024.
Edited material approved by authors: December 31, 2024.
