EQUINE VETERINARY EDUCATION / AE / March 2011 109 Case Reporteve_149 109..118 Three types of anomalous vasculature in the equine umbilical cord S. Wilsher*, J. Ousey, K. Whitwell†, J. S. Crowhurst‡, H. N. Neal‡ and W. R. Allen The Paul Mellon Laboratory of Equine Reproduction (formerly The Equine Fertility Unit); †Equine Pathology Consultancy; and ‡Newmarket Equine Hospital, Suffolk, UK. Keywords: horse; umbilical cord; placenta; umbilical artery; umbilical vein; supernumerary umbilical vessels Summary branches of the aorta. However, some of the blood that enters the right atrium is directed via the right ventricle to Anomalies in the number of major blood vessels in the mix with deoxygenated blood returning from the head umbilical cord are well documented in man and have and myocardium, before heading to the pulmonary trunk been associated with both placental abnormalities and where the greater volume passes through the ductus congenital problems in the neonate. This paper describes 5 arteriosus to the caudal aorta. The lesser volume supplies cases of anomalies in the number of umbilical arteries or the pulmonary vessels of the nonfunctioning fetal lungs. veins within the equine umbilical cord at term. In 4 cases, Most of the blood in the caudal aorta heads back to the anomalies affected vessels in the amniotic part of the the placenta, with arterial branches ensuring that cord, and in one case, vessels in the allantoic part. In all the thoracic and abdominal organs are oxygenated. The the cases placental morphology was essentially normal deoxygenated blood finally leaves the fetus through the and fetal health and post natal development were not paired umbilical arteries, returning to the allantochorion to compromised as a result of the unusual arrangement of become reoxygenated (Fig 1; McGeady et al. 2006). blood vessels within the cord. The equine umbilical cord develops from the convergence of the 2 fetal sacs, the amnion and allantois, Introduction around the remnants of the yolk sac and the vitelline duct to form a cord-like structure by Day 50. Embedded in the connective tissue, and formed from the allantoic In pregnant mammals, the umbilical cord provides the mesoderm, are the umbilical vessels. In ruminants there are route through which the fetal blood carries the nutrients 2 arteries and 2 veins along the whole length of the cord and oxygenated blood to, and all the gaseous and but in other species, such as equids and carnivores, the metabolic waste from, the developing fetus. Since the amniotic portion end of the cord has 2 arteries but only one fetal lungs are not functional in utero it is the umbilical veins vein. However, regardless of the species, only one umbilical which supply oxygenated blood to the fetus. This passes vein persists inside the fetus in late gestation (Fig 1; Latshaw initially through the ductus venosus, the major blood 1987). channel from the placenta through the embryonic liver, to The umbilical cord in the horse comprises a proximal the caudal vena cava (McGeady et al. 2006). This shunt intra-amniotic portion, which is covered by amnion and is remains patent throughout gestation in most domestic attached to the fetus at the umbilicus, and a distal species but, in the horse and pig, it atrophies during allantoic portion covered by allantois that is attached to gestation and blood from the umbilical vein then passes the allantochorion. The amniotic portion of the cord through the sinusoids of the liver en route to the caudal contains 2 umbilical arteries, one umbilical vein, the vena cava. From here the blood enters the right atrium of vitelline vein remnant and the urachus. In the allantoic the heart where most of it is directed through the foramen portion of the cord the 2 major umbilical arteries become ovale into the left atrium. This blood then enters the left increasingly divergent and multibranched towards the ventricle and is pumped throughout the body via the chorion: the 2 umbilical veins returning blood to the fetus aortic arch, with the cardiac musculature and brain tend to lie in close proximity to these arteries. The 2 major receiving highly oxygenated blood from the first 2 veins unite at the proximal end of the allantoic portion of the cord or just inside the amniotic cavity (Fig 2; Whitwell *Corresponding author email: [email protected] and Jeffcott 1975; Schlafer 2004). The allantoic portion of © 2010 EVJ Ltd 110 EQUINE VETERINARY EDUCATION / AE / march 2011 1 42 III 8 the human umbilical cord, particularly the existence of a 3 single umbilical artery (SUA), are well documented (reviews: Baergen 2005; Fox and Sebire 2007). In this paper, 5 cases of anomalies in the major vessels within the term equine umbilical cord are reported. Two IV cases describe the atypical arrangement of the 2 arteries I 9 6 within the umbilical cord, 2 cases detail an increased 5 number of vessels in the amniotic portion of the cord, and the fifth describes an increased number of vessels in the 7 II allantoic portion of the cord. The cases are discussed in relation to the normal development of the feto-placental V circulation and compared to similar conditions in the human infant. Case 1: Atypical arrangement of the umbilical arteries in the umbilical cord Fig 1: A diagrammatic representation of the relationship of the Clinical history umbilical vessels and the fetal circulation in utero. I: heart; II: liver; III: lung; IV: bladder; V: urachus; 1: aorta; 2: ductus arteriosus; 3: foramen ovale; 4: pulmonary arteries; 5: left umbilical vein; A multiparous, 7-year-old Thoroughbred (TB) mare foaled a 6: umbilical arteries; 7: ductus venosus; 8: caudal vena cava; healthy 52 kg colt foal without complication following an 9: portal veins. Redrawn from Rüsse and Sinowatz (1998) and uneventful gestation of 336 days. Fetal development Latshaw (1987). appeared normal as judged by foal birthweight as a percentage of maternal weight (Table 1). Gross examination of the placenta revealed only one major a) Intra-amniotic cord Intra-allantoic cord artery in the amniotic portion of the umbilical cord. Am Retrospective checking of the mare’s breeding records UA revealed that she had been mated only once during UA UV UV oestrus when she exhibited a follicle >35 mm in one ovary. UV UA UA She had subsequently undergone 5 transrectal ultrasound examinations to diagnose and monitor pregnancy on Days Normal cord 13, 19, 27, 52 and 66 after ovulation when development appeared normal in the singleton conceptus. b) In the 2 previous breeding seasons the mare had UV produced healthy colt foals (41.1 and 48 kg, respectively) UA after gestation lengths of 334 days in both instances. The same TB stallion had sired all 3 foals. Normal cord UA Gross placental findings Fig 2: a) Normal morphology of the equine umbilical cord. Note Linear placental measurements fell within the normal that there are 2 umbilical arteries (UA) and one umbilical vein (UV) ranges for TB placentae as reported by Whitwell and in the amniotic portion of the cord, but 2 arteries and 2 veins in the Jeffcott (1975). The placenta was presented with the allantoic portion. A white arrow indicates the urachal opening into the allantoic cavity. The amnion (Am) has been cut off close to the allantoic surface outermost, which was normal in cord so the vessels can be visualised; b) the urachal lumen has appearance. The chorionic (villous) surface appeared been opened to reveal the joining of the 2 umbilical veins. The grossly normal. The placental parameters are listed and direction of flow and oxygenation status of blood in the umbilical compared in Table 1 to previously published data for TB vessels are indicated by the arrows and dashed lines (red denotes oxygenated blood and blue denotes deoxygenated blood). mares. The umbilical cord attachment site to the allantochorion was normal (i.e. between the 2 horns). The the umbilical cord also contains remnants of the yolk sac cord had ruptured naturally as indicated by protrusion of and vitelline vessels as well as a smooth walled cavity, the the wall of an artery from the fetal end of the cord. The infundibulum, a remnant of the extra-embryonic coelom. vascular pattern of the major vessels was type I (K.E. To the authors’ knowledge, apart from an isolated case Whitwell, personal communication in Rossdale and Ricketts of a single umbilical artery (Whitwell 1975), there are no 2002). That is, one vein and artery vascularised the whole other reports of anomalies in vessel number in the equine of the gravid horn while the other vein and artery umbilical cord. In contrast, anomalies in vessel number in vascularised the nongravid horn and uterine body. The © 2010 EVJ Ltd EQUINE VETERINARY EDUCATION / AE / March 2011 111 TABLE 1: Previously published placental and fetal parameters for Thoroughbred and Pony mares compared to those for Cases 1, 2, 3, 4 and 5. Where the placental parameter is outside the 95% range for Thoroughbreds (Cases 1, 3, 4 and 5) and the range† for Ponies (Case 2)from previously reported for the respective breed this is indicated by either an ↓, if the value falls below, or ↑, if the value is above Mean Ϯ s.e. (95% range) of Mean Ϯ s.e. (range) normal TB placentae of normal Pony placentae (Wilsher and Allen 2003, (Allen et al. 2002, n = 7; n = 84; Whitwell and Case 1 Case 3 Case 4 Case 5 Whitwell and Jeffcott§ Case 2 Parameter Jeffcott 1975*, nՆ139) TB mare TB mare TB mare TB mare 1975, n = 10) Pony mare Gestation length (days) 340.5 Ϯ 0.77 (324–359)* 336 345 327 330 324.6 Ϯ 2.97 (312–333)