Umbilical Circulation

Introduction

The fetoplacental circulation, also known as umbilical circuit, with its transport of nutrients, gases, and endocrine signaling, is critical for fetal development. A long tradition of animal experiments has given us indispensable insights into its physiology. However, the introduction of ultrasound techniques enabled studies of the human version of this physiology free from the surgical trauma hampering the experimental procedures. This chapter prioritizes human data where possible, as animal and human physiology are different. For example, fetal lambs have a fundamentally different placenta; four vessels in the umbilical cord; different anatomy of the liver, portal veins, ductus venosus, and intrathoracic inferior vena cava; faster growth; shorter pregnancy; lower hemoglobin; and higher heart rate and temperature than the human fetus.

Anatomy

Technically, the fetoplacental circuit starts in the heart as it ejects blood into the aorta and pulmonary artery, and ends with the inferior vena cava entering the heart ( Fig. 53.1A ). However, the umbilical circulation starts as the umbilical arteries branch from the internal iliac arteries, passing the fetal urinary bladder on both sides to enter the umbilical cord through the umbilical ring. Here the two arteries are bundled with the umbilical vein to communicate with the placenta. The vessels are suspended in Wharton jelly, which prevents external compression of the vessels, and covered with the amniotic membrane to form the free loop of the cord (the amniotic part of the umbilical circuit). At the insertion of the cord in the placenta, the arteries commonly communicate (Hyrtl’s anastomosis) before branching on the amniotic surface of the placenta. The anastomosis equalizes blood pressure and stabilizes the distribution into the smaller arteries in the depths to reach the capillary system of the villi. In the villi, the capillaries communicate extensively with each other before fusing into venules and veins to finally form a single umbilical vein (two umbilical veins in early embryonic development; see Chapter 45 ) that joins the two arteries in the cord on its way to the fetal umbilicus. Here, it enters through the somehow constricting umbilical ring to become the intra-abdominal umbilical vein, embedded in the inferior surface of the liver, and connects with the portal system (see Fig. 53.1B ). During fetal life, the nutritious umbilical venous return feeds the left side of the liver through branches of the left portal system then feeds the shunt ductus venosus that directs blood into the inferior vena cava and foramen ovale. The remainder flows beyond the ductus venosus inlet to merge with blood from the main portal stem and circulate through the right liver lobe ultimately reaching the heart via the hepatic veins and inferior vena cava ( Fig. 53.2 ).

After birth, as the umbilical arteries obliterate and cord is clamped (see “Umbilical Circulation at Birth and Timing of Cord Clamping”), the intra-abdominal umbilical vein obliterates distal to the first portal branches into the left liver lobe (see Fig. 53.2 ), and the entire portal system including the ductus venosus is now supplied from the main portal stem. As for the ductus venosus, 76% obliterate within a week in healthy term neonates, ^, while in premature neonates ^, or neonates with pulmonary hypertension, it may stay open for 2 to 3 weeks.

In singleton pregnancies, 0.5% to 1.0% of the umbilical cords have a single artery. These pregnancies have an increased risk of adverse perinatal outcome including small for gestational age neonates. While conventionally the umbilical cord has a central insertion into the placenta, 6% to 7% have a marginal insertion (<3 cm from the placental border) and 1% to 2% a velamentous insertion into the fetal membranes, both associated with an increased risk of adverse perinatal outcome including prematurity and low birth weight.

The Volume of Blood in the Umbilical Circuit

The fetus circulates a blood volume corresponding to 11% to 12% of its weight, which is considerably higher than the 7% during adult life. The reason is that at any time a large proportion of blood is contained within the placenta. This fraction, however, decreases from 50% at mid-gestation to below 25% near term, according to sheep data ( Fig. 53.3 ). Although the fetal liver and splanchnic circuit have a capacity to accumulate blood volume and act as a buffer within the circulation, the umbilical circuit with the huge placental volume represents a correspondingly larger volume buffer.

Umbilical Blood Flow

Umbilical blood flow (mL/min) is a key determinant for fetal growth, has attracted numerous experimental and clinical studies, and is still today of great physiologic interest but has not fully reached clinical applicability. With improved ultrasound techniques and study designs, a number of studies have confirmed and refined the pioneering studies by Gill and colleagues ^, showing that umbilical blood flow grows steadily during the second half of pregnancy, with some blunting toward term ( Fig. 53.4 ). However, fetuses developing birth weight exceeding the 90th percentile without hyperglycemia have less or no blunting. Although small dimensions impose substantial measurement variation, umbilical flow has been described for gestational weeks 11 to 20.

Before 20 weeks of gestation, umbilical blood flow normalized for fetal weight (mL/min/kg) increases steadily ( Fig. 53.5 ). This hemodynamic development is also reflected in the increasing distribution of fetal cardiac output to the umbilical circuit—that is, from 14% to 21% during 11 to 20 weeks of gestation (see Fig. 53.5 ). These findings in early human pregnancies corroborate previous animal data. These events coincide with establishment of intervillous circulation at the end of the first trimester, which is followed by rapid expansion of the vascular cross-section and a corresponding fall in resistance. ^,

After 20 weeks of gestation, however, the umbilical flow per kilogram of fetal weight declines from 105 to 65 mL/min at term ( Fig. 53.6A ). During gestational weeks 20 to 30, a steady fraction (30%) of the total cardiac output is distributed to the placenta. Beyond 30 weeks, the fraction declines to reach 20% or less before term (see Fig. 53.6B ). In contrast, the fetus maintains a combined cardiac output of 400 mL/min/kg during the entire second half of pregnancy. Thus the fetus seems to have a tight regulation to maintain cardiac output per kilogram of body weight, and at mid-gestation it uses 70% of its cardiac output to perfuse its body as the rest (30%) is directed to the placenta. During the last trimester, 80% is circulating to the body, whereas only 20% is directed to the placenta.

Interestingly, normalized cardiac output is maintained equally well in growth-restricted fetuses, even with the most severe placental compromise ( Fig. 53.7A ), while the fraction distributed to the placenta is significantly reduced and may reach 10% or less in the most severe cases (see Fig. 53.7 , B ). This implies that 90% or more of the blood is recycled within the fetal body without being rejuvenated in the placenta.

Umbilical Artery Hemodynamics

Arterial Pulsation

The pulsation of the umbilical artery blood flow velocity is extensively used in obstetrics because the waveform recorded using Doppler ultrasound indicates the downstream impedance. The waveform is quantified by various indices, the most robust being the pulsatility index ( Fig. 53.8A ). An increased pulsatility index is associated with increased impedance in the umbilical circuit—that is, hemodynamic compromise (see Fig. 53.8B ). ^, However, the relation between the waveform and resistance in the placental bed is not linear. Obliterating half of the fetoplacental vessels may hardly impact the pulsatile waveform, as shown in embolization experiments and mathematical modeling ( Fig. 53.9 ). ^, Part of the explanation is that the resistance to pulsatile flow—that is, impedance, in addition to vascular cross-section and length—is governed by the fluid dynamic determinants of pulsation that include frequency, pressure amplitude, and vessel compliance, as well as viscosity when velocities are low.

The arterial pulse wave consists of three components: pressure, vessel diameter, and blood velocity wave. As the pulse wave travels downstream in the vascular tree, it moves considerably faster than the average blood velocity in the vessel. The stiffer the vessel, the faster the pressure wave travels. In the fetus, it is estimated that the speed climbs from less than 2m/s to 10 m/s within the first 20 cm from the heart. Thus the pressure wave reaches the periphery early and is reflected whenever there is a change of impedance (which is determined by local vessel geometry and distensibility and blood viscosity). The reflected pressure wave interferes with the downstream velocity wave, which is the reason why velocity waves in the umbilical artery indicate details of the downstream vasculature. Conventionally, the reflected wave will hit the downstream wave with a phase shift and cause a velocity deflection because now it is running in the opposite direction of flow ( Fig. 53.10 ). This is particularly seen in the extreme cases of placental compromise, when the umbilical artery end-diastolic velocity is zero or reversed (see Fig. 53.8B ). In the normally developing umbilical vasculature, this reflected pulse-wave interference is less marked, probably signifying the diffuse distribution of a large number of bifurcations causing the various reflected waves to cancel out each other. The blood velocity waveform in the umbilical artery changes to a less pulsatile pattern with advancing gestation, reflecting continued vascular proliferation.