In vitro hemodynamic investigation of the embryonic aortic arch at late gestation

Abstract

This study focuses on the dynamic flow through the fetal aortic arch driven by the concurrent action of right and left ventricles. We created a parametric pulsatile computational fluid dynamics (CFD) model of the fetal aortic junction with physiologic vessel geometries. To gain a better biophysical understanding, an in vitro experimental fetal flow loop for flow visualization was constructed for identical CFD conditions. CFD and in vitro experimental results were comparable. Swirling flow during the acceleration phase of the cardiac cycle and unidirectional flow following mid-deceleration phase were observed in pulmonary arteries (PA), head-neck vessels, and descending aorta. Right-to-left (oxygenated) blood flowed through the ductus arteriosus (DA) posterior relative to the antegrade left ventricular outflow tract (LVOT) stream and resembled jet flow. LVOT and right ventricular outflow tract flow mixing had not completed until approximately 3.5 descending aorta diameters downstream of the DA insertion into the aortic arch. Normal arch model flow patterns were then compared to flow patterns of four common congenital heart malformations that include aortic arch anomalies. Weak oscillatory reversing flow through the DA junction was observed only for the Tetralogy of Fallot configuration. PA and hypoplastic left heart syndrome configurations demonstrated complex, abnormal flow patterns in the PAs and head-neck vessels. Aortic coarctation resulted in large-scale recirculating flow in the aortic arch proximal to the DA. Intravascular flow patterns spatially correlated with abnormal vascular structures consistent with the paradigm that abnormal intravascular flow patterns associated with congenital heart disease influence vascular growth and function.

Figure 1

Fetal aortic arch junction. The parametric solid computer aided design model in (a) with the normal vessel dimensions, given in parenthesis in millimeters. The glass replica of this model is shown in (b) which is used in flow visualization experiments. This idealized model has physiological vessel dimensions and flow rates for human fetus at late gestation. (DA: Ductus arteriosus, LVOT: Left ventricular outflow tract, RVOT: Right ventricular outflow tract, DAo: Descending aorta, LPA: Left pulmonary artery, RPA: Right pulmonary artery) Vessel diameters (LVOT, RVOT, DA, PA, DAo) in mm used for congenital morphologies are as follows: HLHS (1.5, 12, 6, 10-7, 7.5), TOF (12, 5, 5, 8-5, 7.5) and PAT (0, 12, 5, 9-6, 7.5) respectively. Corresponding morphologies span a hypoplastic LVOT (HLHS) to a hypoplastic RVOT (PAT), see also Fig 7a.

Figure 2

(a) Computational and experimental flow waveforms specified and measured. The difference between these mean flow rates are less than 1%. CFD curve had no backflow. (b) Reynolds and Womersely numbers in major arterial vessels during late gestation. While the Reynolds numbers remain low due to the distributed total cardiac output between right and left hearts, unsteady effects are not negligible. Cardiac output data is abstracted from reference (Gadelha-Costa et al, 2007).

Figure 3

Snapshots of pulmonary artery flow structures. LEFT: Particle pathlines during acceleration and deceleration phases calculated from the pulsatile CFD results originating from a section at the LPA root are plotted. MIDDLE: Instantaneous streamlines are plotted for selected cardiac phases. RIGHT: Swirling flow visualized experimentally at the steady mean flow condition. (See Supplemental Movies 1 and 2)

Figure 4

Pulsatile flow visualization in the normal fetal aortic arch at acceleration and mid deceleration phases. Flow pathlines are plotted for both CFD and experiments for comparison at the same instant (See also Supplemental Movie 3). During deceleration separation bubbles are observed for all head-neck vessels, highlighted with arrows.

Figure 5

Comparison of swirling flow patterns in the descending fetal aorta observed in CFD and in vitro experiments during the peak flow and mid-deceleration phases. Flow pathlines are visualized both for CFD computations and experiments. Cross-sectional flow streamlines are also shown as inserts featuring instant flow swirl.

Figure 6

Computed 3D flow streaklines illustrates the DA shunting Orange and Green labeled streams corresponds to LVOT and RVOT flows respectively. RVOT and LVOT flows remain separated for a distance downstream of ductus as illustrated with the arrow.

Figure 7

(a) Instantaneous 3D fetal aortic flows of idealized CFD models of the normal and the three common congenital heart defect templates during mid-deceleration phase. Red and blue color corresponds to high and low flow velocities as graded in the upper right corner scale in m/s. Reversed and high DA flows for PAT and HLHS cases are illustrated. Flow fields over one cardiac cycle are provided in Supplemental Movies (6 to 9). (b) Average flow waveforms calculated through the ductus arteriosus. Positive values indicate pulmonary perfusion. Only TOF featured a very weak backflow. All other cases were unidirectional. HLHS: Hypoplastic left heart syndrome, TOF: Tetralogy of Fallot, PAT: Pulmonary Atresia.