New Advances in Cardiac Magnetic Resonance Imaging of Congenital Heart Disease

Abstract

Cardiac magnetic resonance (CMR) is an indispensable second-line tool, next to CT (computed tomography), in the evaluation and follow-up of congenital heart disease in adults and children, as a complement to echocardiography, without the inconvenience of X-rays. This imaging requires a long examination time and good cooperation from the patient to achieve good apnea, or the use of general anesthesia in children under 8 years of age. In this chapter, we summarize the recent advances in CMR sequences, notably the four-dimensional (4D) flow, in software and hardware technologies that allow a wider use, thanks to the simplification of the examination protocols and the decrease of the acquisition time.

1. Introduction

Significant improvements in the diagnosis and management of patients with congenital heart disease (CHD) have led to increased number of patients surviving to adulthood [1]. These patients require lifelong noninvasive follow-up to detect long-term complications [2, 3].

Since 2020, the ACC/AH and the ESC published [4] the new guidelines for the management of adult CHD [5].

CMR is the only imaging modality offering in a single time an excellent anatomical and functional information of the heart [6, 7]. Long follow-up with repetitive CMR imaging is reasonable for its high reproducibility and safety compared to CT and catheterization, in the young population.

This imaging requires a long examination time and good cooperation from the patient to achieve good apnea, or the use of general anesthesia in young children. The use of advanced CMR sequences as such a 4D flow is a good option for improving this limitation.

Novel emerging techniques especially advanced flow evaluation and reduced acquisition and post-processing times [8] are a major step forward in the evaluation of CHD with flow perturbations [9].

2. 4D flow

4D flow CMR refers to phase-contrast CMR with flow-encoding in all three spatial directions, in typical transverse, sagittal, and coronal planes and resolved to the three dimensions of space and the dimension of time along the cardiac cycle. It allows a velocity assessment in the whole heart and great vessels [10] with prospective or retrospective electrocardiogram (ECG) gating. The images obtained are displayed in a colored representation of the flow patterns.

The 4D flow enables a flow analysis in any vessel section in a single acquisition, which is especially relevant in complex CHD.

4D flow CMR requires a reliable ECG with detectable R-wave. To cover the entire aorta, it is important that the coils are positioned high enough to explore certain aortic pathologies. The scans can be relatively long and it is important to inform the patient before.

4D flow CMR employs spoiled gradient echo sequences with short TR for rapid imaging with the generation of PC angiograms without the need for an external contrast agent. According to the 4D flow cardiovascular magnetic resonance consensus statement 2023, the recommended spatial resolution in adult vessels is 2.5–3 mm³, 2–2.5 mm³ in pediatric vessels, and 30–50 ms for temporal resolution. A flip angle of 7° is advised if non-contrast acquisition [11].

The advantage of 4D flow CMR is the retrospective analysis of the blood flow through any planes of interest across the 3D volume.

Moreover, the analysis of advanced hemodynamic parameters as kinetic energy (KE) and wall shear stress (WSS) has become possible [12, 13].

4d flow allows precise assessment in a variety of clinical situations, including evaluation of the QP/QS ratio, collateral flow, and valve regurgitation.

Retrospective cardiac gating is preferred, to analyze the flow in systole and diastole.

Respiratory gating is used to avoid motion artifacts; respiratory motion compensation is a good alternative if it is available.

As with 2D, 4D flow requires a close value of real peak velocity to avoid aliasing. A VENC of 120–150 cm/s is sufficient in the absence of stenosis; otherwise it should be increased to the peak velocity expected by other methods, such as echocardiography, and using post-processing tools with anti-aliasing correction should be considered.

• Resolution: Acquired voxel size according to JCMR consensus document [11] for intracardiac flow is 3 mm or less. In small children, higher spatial resolution is recommended, because of the smaller FOV (field of view).

3. Application

3.1 Fontan repair

The Fontan operation is the last stage in the palliative treatment in univentricular heart [14].

The main goal of CMR is the assessment of the ventricle function, possible valvular regurgitation, the patency of the Fontan pathway, and the presence of collateral flow [15].

Various manifestations can occur such as protein-losing enteropathy, plastic bronchitis, interstitial pulmonary edema, pleuro-pericardial effusion, and ascites. MR is able to characterize lymphatic perfusion abnormalities using static and dynamic sequences, which will not be detailed in this chapter.

Aortic forward flow should be equal to total systemic venous return and to total pulmonary venous return. The divergence in flows indicates the presence of regurgitant lesions, patent fenestration, or significant systemic-to-collateral [16].

Late gadolinium enhancement (LGE) imaging is indicated in cases of recent degradation in cardiac function, suspicion of thrombus formation, or new onset of complex arrhythmias to detect the presence and extension of myocardial fibrosis. Contrast-enhanced (CE-MRA) in the venous phase allows the assessment of the permeability of the Fontan circuit. Moreover, 4D flow imaging allows the quantification of any obstruction based on distribution patterns of caval or pulmonary artery flows (Figure 1) [16].

Figure 1.

4D flow MRI in a total cavo-pulmonary connection with flow distribution 70% into the RPA and 30% in LPA. RPA: Right pulmonary artery, LPA: Left pulmonary artery.

4. Tetralogy of Fallot (TOF)

An accurate assessment of pulmonary valve regurgitation (PVR) is essential prior to pulmonary revalvulation (PR). This assessment is better performed using 4D flow CMR because of the possibility to correct for through-plane motion of the valve and flow angulation. Advanced flow parameters such as ventricular kinetic energy (KE) represent a novel tool to assess cardiac function; KE represents the amount of energy present in the blood flow due to movement and is considered a good marker of ventricular efficiency; it is calculated using the following equation: KE = ½mv² where m represents the mass (the voxel volume multiplied by the density of blood) and v represents the velocity of each voxel, determined from the 4D flow. Jeong found that the KE was abnormal in TOF patients compared to in healthy controls [17].

According to the current CMR criteria, a large percentage of patients continue to experience symptoms of the classic complications observed in patients not undergoing PR, such us ventricular arrhythmias and heart failure [18].

4D flow provides a more accurate assessment of PV regurgitant flow, which may lead to better timing of revalvulation.

Several studies show that turbulent kinetic energy in the right ventricle was higher in patients with TOF than in healthy controls, mainly in the RVOT [17, 19, 20].

Jeong demonstrated that KE is an earlier indicator of cardiac dysfunction than classic parameters such us EDVI, ESVI, and EF.

Furthermore, patients with TOF may have pulmonary valve or branch stenosis. Consequently, analysis of PA flow based on 2D PC CMR plane is prone to error. Geiger and Francois [21] found that TOF patients present helical flow patterns in the pulmonary arteries [22].

These findings have been reported by Hu et al. [23]. They found that vortices were predominantly present in the main PA and helical flow patterns were predominantly present in the right PA, which was associated with systolic energy loss in the right PA and increased RV dimensions, suggesting impaired ventricular–arterial coupling.

5. Aortic diseases

In the aorta, aortic flow was assessed in all three segments, on the ascending, transverse, and descending aorta, in a plane perpendicular to the aortic axis.

The advantage of the 4D flow is that the plans can be placed after the acquisition.

Vorticity and helicity are two parameters that provide information about the rotational movement of blood flow.

Vorticity describes the rotation of a fluid particle around the same axis as well as around its own axis, which describes a curved movement.

Helicity is determined from vorticity and the principal component of flow velocity, which determines the direction of flow.

In aorta, the flow has a helical pattern at the end of systole, in the upper aortic arch as has been described by Kilner [24]; (Figure 2) it allows the preservation of laminar flow in the aortic arch. In aortic pathological conditions such as aneurysms, aortic bicuspidi, coarctation, or dissection, rotational flow is abnormal.

Figure 2.

4D flow CMR of the normal aorta showing the direction of flow in all three phases of systole (early, peak, and end systole).

6. Three-dimensional printing and virtual reality

Three-dimensional (3D) printing technology has become an attractive tool for creating patient-specific anatomical models (Figure 3). Its role in clinical decision and patient management in complex CHD is increasing.

Figure 3.

3D-printed models of transposition of the great arteries and arterial switch operation. Ao, aorta; SVC, superior vena cava; PT, pulmonary trunk; LV, left ventricle; RA, right atrium; RV, right ventricle.

Numerous studies have demonstrated superior advantages of 3D-printed models over the traditional 2D and 3D image reconstructions, enhancing the perception of distances and spatial configuration of the complex cardiac morphology and therefore facilitating the surgical planning [25, 26, 27].

A multicenter study [28] showed that the use of 3D-printed heart CHD models enabled surgical decisions to be modified in around 50% of cases.

In a similar way, other studies have confirmed the usefulness of 3D-printed cardiac models to guide surgical procedures in patients with CHD [20, 29, 30, 31].

Gomez-Ciriza et al. [32] reported their experience of 7 years in which 3D-printed heart models were able tomodify the surgical decision in 48% of cases.

However, the large application of 3D printing technology in pediatric cardiology practice is still limited by some barriers.

Geographic location: A recent international survey [33] has found that the ability to access 3D printing technology differs from region to region.

The cost of printing materials is another factor that limits its application in many practices, especially soft and elastic materials (high-cost 3D-printed models) with tissue properties similar to normal cardiovascular tissues.

Another limitation of this model is the long time required from image reconstruction to printing and cleaning of the models.

If 3D printing is unavailable, virtual reality (VR) could be a promising technique in clinical application and medical education for CHD. Raimondil and colleagues [34] noticed that the median time to elaborate VR models was only 5 min, which is interesting compared to 3D printing models, which required a long time (8 hours).

7. Interventional CMR

Invasive cardiovascular magnetic resonance imaging (CMR) of cardiac catheterization is a better alternative to fluoroscopy, which has been the gold standard in the assessment of patients with congenital heart disease (CHD). It provides real-time anatomical visualization of the cardiovascular structures [35, 36, 37] and the guidance for hemodynamic data without the radiation exposure. The harmful effects of repeated use of X-rays in this population have been increasingly debated in recent years. Prolonged exposure to radiation would be associated with increased risk of cancer in adult patients followed for congenital heart disease [38, 39]. Then, interventional CMR catheterization is a good alternative without ionizing radiation in children, in whom a repetitive hemodynamic assessment would be necessary.

Conditioned catheters and guidewires with gadolinium-filled balloon have been used in CMR-guided cardiac catheterization [40, 41, 42].

A few centers reported their experiences with invasive CMR [35, 43, 44, 45, 46, 47, 48] for diagnostic and interventional procedures under CMR guidance such as CoA, and Fontan fenestration test occlusion, and pulmonary vein access [49].

ICMR is currently performed in several centers [50], in patients with CHD patients before surgery or in the postoperative follow-up, for diagnostic purposes, in particular catheterization of the right heart in cases of pulmonary hypertension or a more detailed hemodynamic study in complex congenital heart disease (pre-Fontan study, or Fontan fenestration test occlusion, for example,) or for therapeutic purposes (closure of an intercavitary shunt).

The advantage of ICMR is its ability to measure cardiac output and the QP/QS ratio by phase contrast, which have proved to be more reliable than thermodilution, which can be distorted by the presence of a valve leak, or Fick’s principle, which gives an estimated rather than measured VO2 value, and at rest rather than during exercise or stress.

In addition, MRI allows ventricular and atrial volumes, EF and functional analysis, and tissue characterization.

Reddy [49] demonstrates the potential of iCMR in diagnostic right and left heart catheterization, CoA diagnosis, and Fontan fenestration occlusion hemodynamic testing.

The balloon attached to the tip of the catheter was filled with diluted gadolinium and guided using a conditioned guide toward the structures to be evaluated hemodynamically, using the real-time sequence (Figure 4).

Figure 4.

Series showing a MR-conditional guidewire (a–b solid white arrow) used to guide the gadolinium-filled balloon (dashed white arrow) for a RHC and LHC (c), Fontan fenestration test occlusion, and measure (D–G) of the pulmonary venous saturation in the LA. F: Gadolinium-filled balloon crossing a severe CoA with the assistance of an MR-conditional guidewire. Image courtesy of Surendranath R. Veeram Reddy and Yousef Arar, pediatric cardiology, Children’s medical center Dallas, 1935 Medical District Dr., Dallas, TX, 75235, USA.

Recently, use of fully insulated nitinol guidewires is feasible in low-SAR and low-field imaging [51, 52].

In the electrophysiology field, CMR allows complete delineation of the atrial anatomy and detection of fibrosis of the left atrium and intra-atrial thrombosis. CMR-guided ablations in particular, cavotricuspid isthmus (CTI) ablation by real-time iCMR guidance is increasingly performed in different centers with similar results to conventional fluoroscopy-guided ablation [53].

8. Conclusion

The new techniques developed over the last decade in cardiac MRI of CHD are promising, offering reduced acquisition and post-processing times while exploring multiple flows in the same examination, thanks to 4D flow, radiation-free diagnostic and therapeutic procedures with ICMR, and accurate anatomical description elaborated by 3D printing in complex CHD. These new tools are currently used in only a few centers and should be accessible in the coming years to the various magnetic resonance imaging centers.