Differences in pulmonary arterial flow hemodynamics between children and adults with pulmonary arterial hypertension as assessed by 4D-flow CMR studies

Abstract

Despite different developmental and pathological processes affecting lung vascular remodeling in both patient populations, differences in 4D MRI findings between children and adults with PAH have not been studied. The purpose of this study was to compare flow hemodynamic state, including flow-mediated shear forces, between pediatric and adult patients with PAH matched by severity of pulmonary vascular resistance index (PVRi). Adults (n = 10) and children (n = 10) with PAH matched by pulmonary vascular resistance index (PVRi) and healthy adult (n = 10) and pediatric (n = 10) subjects underwent comprehensive 4D-flow MRI to assess peak systolic wall shear stress (WSS_max) measured in the main (MPA), right (RPA), and left pulmonary arteries (LPA), viscous energy loss (E_L) along the MPA-RPA and MPA-LPA tract, and qualitative analysis of secondary flow hemodynamics. WSS_max was decreased in all pulmonary vessels in children with PAH when compared with the same age group (all P < 0.05). Similarly, WSS_max was decreased in all pulmonary vessels in adult PAH patients when compared with healthy adult subjects (all P < 0.01). Average E_L was increased in adult patients with PAH when compared with the same age group along both MPA-RPA (P = 0.020) and MPA-LPA (P = 0.025) tracts. There were no differences in E_L indices between adults and pediatric patients. Children and adult patients with PAH have decreased shear hemodynamic forces. However, pathological flow hemodynamic formations appear to be more consistent in adult patients, whereas flow hemodynamic abnormalities appear to be more variable in children with PAH for comparable severity of PVRi. NEW & NOTEWORTHY Both children and adult patients with PAH have decreased shear hemodynamic forces inside the pulmonary arteries associated with the degree of vessel dilation and stiffness. These differences also exist between healthy normotensive children and adults. However, pathological flow hemodynamic formations appear to more uniform in adult patients, whereas in children with PAH flow, hemodynamic abnormalities appear to be more variable. Pathological flow formations appear not to have a major effect on viscous energy loss associated with the flow conduction through proximal pulmonary arteries.

Keywords: cardiac magnetic resonance; flow; magnetic resonance imaging; pediatric and adult; pulmonary arterial hypertension.

Fig. 1.

The postprocessing pipeline for the calculation of hemodynamic wall shear stress (WSS) using 4D-flow MRI. A: after segmentation of the right ventricular (RV) outflow tract and proximal pulmonary arteries, flow analysis was achieved using interactive path line visualization. Principle flow hemodynamic curve was generated by positioning the plane of analysis into the mid-main pulmonary artery (MPA). B: visualization of calculated WSS map through the same segmented region of interest. WSS was measured in the standardized fashion in the mid-MPA and 3 cm from the center of the bifurcation in each branch pulmonary artery. LPA; left pulmonary artery; RPA, right pulmonary artery.

Fig. 2.

Viscous energy loss (E_L) analysis scheme in pulmonary vasculature. A: from the segmented 3-dimentional contour depicting the proximal pulmonary vasculature, E_L was calculated along 2 standardized anatomic trajectories. B: the first trajectory, main pulmonary artery (MPA)-right pulmonary artery (RPA), was defined by the centerline placement from the pulmonary valve 5 cm from the center of the bifurcation. Identical approach was applied for the MPA-left pulmonary artery (LPA) trajectory. C: mean intensity projection of the E_L field within each trajectory, with the E_L waveform depicting the amount of the viscous energy loss at various time through cardiac cycle.

Fig. 3.

Hemodynamic wall shear stress (WSS) measured in the proximal pulmonary arteries. A–C: plots depicting the variability in maximum systolic WSS (WSS_max) between all considered groups revealed significantly decreased WSS_max between pulmonary arterial hypertension (PAH) and control group in each age group. Additionally, there was a difference in time-averaged WSS (WSS_TA) between age-specific groups in respective PAH and control groups when the branch pulmonary arteries were considered. D–F: identical plots for WSS_TA.

Fig. 4.

Associations between peak (maximum) systolic wall shear stress (WSS_max) and the primary determinants of WSS, vessel diameter (A) and peak flow velocity (B), measured in the main pulmonary artery (MPA). Both correlations obeyed the relationship between WSS, vessel size, and flow velocity as dictated by steady-state Haagen-Poisseuille equation. C: positive correlation existed between the relative area change (RAC) and WSS_max. PAH, pulmonary arterial hypertension.

Fig. 5.

Summary of viscous energy loss (E_L) measures across all considered groups. There were no differences in maximum E_L along either the main pulmonary artery (MPA)-right pulmonary artery (RPA) (A) or MPA-left pulmonary artery (LPA) (B) tracts. However, there was a higher average E_L in adult pulmonary arterial hypertension (PAH) patients when compared with normotensive adults along both the MPA-RPA (C) and MPA-LPA (D) tracts.

Fig. 6.

Summary of correlation analyses between conventional markers of pulmonary arterial hypertension severity [trans-annular plane systolic excursion (TAPSE) and brain natriuretic peptide (BNP)] and measured 4D-flow hemodynamic indices. TAPSE showed a mild but not significant trend with peak (maximum) systolic wall shear stress (WSS_max) measured in the main pulmonary artery (MPA) (A) and no relationship with viscous energy loss (E_L) measured along the MPA-right pulmonary artery (RPA) tract (B). Similarly, we did not find any relationships between the BNP levels and WSS_max (C) or between BNP and E_L (D). BNP values were natural log transformed.

Fig. 7.

Summary of observed qualitative flow hemodynamic features. A and B: all healthy pediatric and adult subjects revealed normal flow through pulmonary arteries without any secondary flow features or disturbances as visualized by cohesive path lines in representative pediatric (A) and adult (B) subjects. C and D: prominent large-scale vortices were present in 50% of children with pulmonary arterial hypertension (C) and present in all adult patients (D). E: different representation of vortex structure from the sagittal view depicting path lines forming along the dilated main pulmonary artery (MPA) lumen (left), with artistic representation of streamlines depicting the flow trajectory from the right ventricular (RV) outflow tract to branch pulmonary arteries (middle) and velocity mean intensity projection revealing the flow acceleration as part of the vortex formation (right). mPAP, mean pulmonary arterial pressure; PVRi, pulmonary vascular resistance index.

Fig. 8.

Typical formation of the right pulmonary artery (RPA) helix in a representative adult patient. A–D: the origin of the clockwise RPA helix begins at the main pulmonary artery (MPA) vortex diffusing through the RPA ostium and spirals distally throughout systole.

Fig. 9.

Representative cases of children with moderate (A) and severe (B) pulmonary arterial hypertension (PAH) with normal flow pattern without any formation of vortices and helices in pulmonary arteries despite noticeable main pulmonary artery (MPA) luminal dilation. mPAP, mean pulmonary arterial pressure.