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This paper aims to provide information and explanations regarding the clinically relevant options, strengths, and limitations of cardiovascular magnetic resonance (CMR) in relation to adults with congenital heart disease (CHD). Cardiovascular magnetic resonance can provide assessments of anatomical connections, biventricular function, myocardial viability, measurements of flow, angiography, and more, without ionizing radiation. It should be regarded as a necessary facility in a centre specializing in the care of adults with CHD. Also, those using CMR to investigate acquired heart disease should be able to recognize and evaluate previously unsuspected CHD such as septal defects, anomalously connected pulmonary veins, or double-chambered right ventricle. To realize its full potential and to avoid pitfalls, however, CMR of CHD requires training and experience. Appropriate pathophysiological understanding is needed to evaluate cardiovascular function after surgery for tetralogy of Fallot, transposition of the great arteries, and after Fontan operations. For these and other complex CHD, CMR should be undertaken by specialists committed to long-term collaboration with the clinicians and surgeons managing the patients. We provide a table of CMR acquisition protocols in relation to CHD categories as a guide towards appropriate use of this uniquely versatile imaging modality.
This is a consensus document, commissioned, and approved by the Nucleus members of the European Society of Cardiology Working Groups for cardiovascular magnetic resonance (CMR) and grown-up congenital heart disease (GUCH). Its aim is to provide information and explanations regarding the clinically relevant options, strengths, and limitations of CMR in adult congenital heart disease (ACHD). It is based on the experience of the authors supported, where available, by references to published research, and should be read in conjunction with previously published ‘Clinical indications for cardiovascular magnetic resonance’.1
Advances in paediatric cardiology and cardiac surgery have enabled the survival into adulthood of most patients born with congenital cardiovascular malformations. This has led to the establishment of the cardiological sub-specialty of ACHD or GUCH.2,3 Many ACHD/GUCH patients have undergone palliative or reparative surgery earlier in life.4 The operations performed for more complex malformations are rarely curative, in which case lifelong follow-up is generally required to optimize the quality and span of life. As patients survive into adulthood, they may need intervention or surgery for residual haemodynamic lesions, they are at risk of arrythmias secondary to structural heart disease, and they are also susceptible to acquired heart disease. It is important for imaging specialists to understand the underlying malformations, the evolving operative procedures used,5,6 the possible complications, and the questions that need to be addressed for decision making on management or re-intervention.
The versatility and comprehensiveness of CMR7,8 offers numerous investigative possibilities, but this also presents challenges. The relatively high costs of CMR should be weighed against the costs of less fully informed management.
Although echocardiography remains the first line of investigation,48 CMR can contribute to the measurement of regurgitation and the assessment of myocardial or other pathology associated with heart valve disease (Table 1; see also online supplementary notes to Table 1). In patients with bicuspid aortic valve (AoV), it allows assessment of any ascending aortic ectasia, aneurysm, or dissection. Regurgitant or stenotic jets are visible on cine imaging, although appearances depend on the jet size and characteristics and on the relative location and orientation of the imaging slice. The visibility extent of a jet does not necessarily relate to the severity of a lesion. Planimetry of an orifice, or of the cross-section of the jet immediately downstream of the orifice, is feasible in some but not all cases, depending on the structure of the jet and the relative thickness and location of the imaging slice. Jet velocity mapping can contribute to quantification of stenosis, but velocities may be underestimated if the slice is not optimally located, or if the coherent core of the jet is too narrow or fragmented to contain several whole voxels. Quantification of regurgitation of the inflow valves is feasible using ventricular stroke volume difference in the case of a single valve lesion, or by subtraction of the outflow volume, measured by mapping velocities through a plane transecting the relevant great artery, from the corresponding ventricular stroke volume.43 For identification of tethering, prolapse or failure of coaptation of all parts of the mitral (or tricuspid) leaflets, a contiguous stack of cine images aligned perpendicular to the central part of the line of coaptation is recommended.49,50
The commonest complications are stenosis or regurgitation of the RV-to-PA homograft conduit. Stenosis may be due to shrinkage and calcification of the homograft tube, valve, or suture lines. Any jet formation should be visualized by cine imaging and quantified by jet velocity mapping, and regurgitation measured by through-plane velocity mapping.51,52 The autograft valve in the aortic position should also be assessed for possible dilatation and regurgitation particularly in the second decade after operation.53 Possible sub-valvular pseudo-aneurym formation at the proximal suture line should be sought. Visualization of the re-implanted coronary arteries may be included, using a 3D steady state free precession (SSFP) acquisition. If there is a question of post-surgical LV ischaemia or regional wall motion abnormality, perfusion imaging, and/or LGE may be considered.
Cardiovascular magnetic resonance allows assessment of restenosis or aneurysm formation in the region of coarctation repair, as well as any associated pathology such as stenosis or regurgitation of a bicuspid AoV, aortopathy, or LV hypertrophy.54 Cardiovascular magnetic resonance is also helpful with a view to balloon dilatation and stenting or surgery,55,56 with contrast enhanced angiography providing 3D visualization of arch geometry, any aneurysm formation or collateral vessels. After stent placement, depending on the composition of the stent material, CT may provide a more effective assessment and should be considered 3 months after such an intervention. Collateral flow can be quantified by comparing through-plane measurements of flow immediately proximal to the stenosis and at the level of the diaphragm. A decrease of ≥10% is expected physiologically, whereas an increase implies collateral flow rejoining the descending thoracic aorta.57 The aortic arch with coarctation may not lie in a single plane, and when using cine imaging and velocity mapping, it is necessary to identify planes best suited for the depiction and measurement of any jet flow through the coarctation. The presence of diastolic prolongation of forward flow, or a diastolic tail, is a useful sign of significant (re-)coarctation, and can be demonstrated by plotting a velocity–time curve of jet flow beyond the coarctation.58 Berry aneurysms of the circle of Willis or other cerebral vessels occur in up to 10% of patients with coarctation bearing the risk of rupture.59 As rupture of a cerebral aneurysm is associated with high mortality, screening for cerebrovascular aneurysms is possible by an additional magnetic resonance imaging study which may be advisable if symptoms develop.
Cardiovascular magnetic resonance studies allow measurement of the aortic root and of any aortic regurgitation. They allow measurements of the entire aorta and its major branches and of ventricular and mitral valve function. It is important to check for aortic dissection, which may be small and focal, for example by using a 3D contrast enhanced magnetic resonance or b-SSFP acquisition. Moreover, CMR can detect abnormal aortic elastic properties in affected patients before dilation occurs.60–62 Magnetic resonance imaging of the lumbosacral spine may be used to identify dural ectasia.63 Cerebral contrast enhanced magnetic resonance can be helpful in patients with Loeys-Dietz syndrome.
A stack of transaxial cines, supplemented by four-chamber and other oblique cines, is recommended for visualizing the RA–RV anatomy in Ebstein patients. Transaxial cines may be suitable for volume measurements of the functional part of the Ebstein RV, which may be hard to delineate in short-axis slices. In spite of atrialization, higher RV volumes than normal may be found in the presence of severe tricuspid regurgitation. The severity of tricuspid regurgitation can be assessed using through-plane velocity mapping, the VENC typically set at 250 cm/s, to depict the cross-section of the regurgitant stream through a plane transecting the jet immediately on the atrial side of the defect. A tricuspid regurgitation jet cross-section, reflecting the regurgitant defect, of 6 × 6 mm or more can be regarded as severe. An atrial septal defect, due to distension and gaping of a PFO, can be present in ~50% of adult Ebstein patients and should be sought with an atrial short-axis cine stack. If present, the resting shunt can be measured by aortic and pulmonary velocity mapping. Cines may show diastolic compression of the LV by the dilated right heart, which can impair LV filling and so limit the cardiac output.
Cardiovascular magnetic resonance has important contributions to make in the assessment and follow-up of adults with repaired ToF64 and related conditions,65,66 including those with RV–PA conduits. Cardiovascular magnetic resonance measurements of RV and LV function (Figure 1), any regional wall motion abnormalities, PR (Figure 2), RVOT obstruction, conduit or PA stenoses, and possible residual shunting all contribute to decisions on management, notably the possibility of pulmonary valve replacement for PR. The pathophysiology of PR differs from that of aortic regurgitation. Free PR, with little or no effective valve function, is common after repair of ToF. It may be tolerated without symptoms for decades and is typically associated with a regurgitant fraction of ~35–45%,67 which should also be recorded as an indexed regurgitant volume.68 However, RV dysfunction, arrhythmia, and premature death can result, with respect to which CMR late gadolinium imaging may contribute to risk stratification.16 In most centres, pulmonary valve replacement is considered in such patients, but when to operate remains controversial, particularly if the patient is asymptomatic and bearing in mind that a homograft replacement may only function effectively for 15 or 20 years, or less.69–72 Once a conduit is in position, however, progressive stenosis or regurgitation may be treatable by percutaneous placement of a stented valve within the relatively rigid tube of the conduit.73,74 Cardiovascular magnetic resonance, with contrast angiography, has a role in the selection of patients for such procedures, but so also has CT, which allows the visualization of calcium and the clear delineation the coronary arteries relative to a previously placed conduit.
Studies by Therrien et al.75 and Oosterhof et al.76 compared CMR measurements of RV volumes before and after surgical pulmonary valve replacement. Both groups found reductions of RV volumes after surgery. However, patients with pre-operative indexed RV end-diastolic volumes above 170 mL/m2 (or above 160 mL/m2 in Osterhof's study) and end-systolic volumes over 85 mL/m2 (or over 82 mL/m2) failed to recover to the normal RV volume range. Although this may be taken as a guide to RV volumes that should not be exceeded when waiting to replace a pulmonary valve, there are more factors to be considered. Even in the absence of an effective pulmonary valve, the amount of regurgitation depends on factors upstream and downstream. In occasional cases, the regurgitant fraction can exceed 50%.77 This may be attributable to an unusually large and compliant RV, a large and compliant pulmonary trunk and PA branches whose recoil contributes to the regurgitation,78 branch PA stenosis or elevated peripheral resistance limiting the distal escape of flow, or combinations of these.79 In the case of unilateral branch PA stenosis, comparison of right pulmonary artery and left pulmonary artery flow volumes can be informative. Contrast enhanced 3D angiography may be used for the visualization of PA branch stenosis, and appropriately aligned cines can visualize jet formation and the reduced systolic expansion of PA branches distal to a stenosis that is obstructive enough to require relief, either percutaneously or at the time of surgery. Measurements of relative branch PA flow and the visualization of distal PA expansion may also contribute to the assessment of patency after stent placement. Tricuspid regurgitation needs to be identified and assessed, as does any residual ventricular septal defect (VSD) patch leak and consequent shunting. Global and regional LV function, and any aortic root dilatation or regurgitation, also need assessment.80 In summary, the evaluation of repaired ToF requires thorough assessment of the left and right heart, extending to the branch PAs and ascending aorta.
Results from obstructing muscular bands or ridges between the hypertrophied body or sinus of the RV and the non-hypertrophied infundibulum. It is usually associated with a VSD into the higher pressure RV sinus, close to the tricuspid valve, and may progress during adulthood. It should be possible to identify double-chambered right ventricle (DCRV) echocardiographically, although limited visualization may make it hard to distinguish between a jet through a VSD, the sub-infundibular stenosis and possible infundibular or pulmonary valve stenosis. Cardiovascular magnetic resonance can help to differentiate between these, although flow through the VSD can be hard to detect. The sub-infundibular origin of a DCRV jet, directed into the non-hypertrophied and non-obstructive infundibulum, is generally visible in routine basal short-axis cines.81
Contrast enhanced 3D CMR angiography is valuable for delineation of all sources of pulmonary blood supply prior to surgical or transcatheter procedures in patients with major aortopulmonary collateral arteries associated with severe pulmonary stenosis or atresia.82 However, CT angiography is likely to depict small vessels more clearly.
Cardiovascular magnetic resonance allows assessment of RV size and function, the size of the main and branch pulmonary arteries, flow measurement in the aorta or main PA for calculation of indexed cardiac output, and to identify anomalies that might contribute to pulmonary hypertension such as patent ductus arteriosus (PDA) or VSD.83 Contrast enhanced angiography may be used for the identification of thrombo-embolic disease or aorto-pulmonary collateral vessels, although contrast CT offers superior resolution in a shorter time, which may matter in patients with limited breath-holding ability.
Cardiovascular magnetic resonance can assess questions remaining, after echocardiography, about the nature of the lesion, the amount of shunting,43 biventricular size and function, and to detect associated anomalies, notably the possibility of anomalous pulmonary venous drainage.84–86 Flow through the AoV represents Qs when there is an intracardiac left to right shunt, but Qp when the shunt is through a PDA, with the inverse applying to flow in the pulmonary trunk.43
Cardiovascular magnetic resonance can assess the atrial pathways and systemic RV function.87 With experience, cines and velocity maps can be aligned with respect to systemic and pulmonary venous atrial pathways.66 Comprehensive coverage can, however, be achieved using a stack of contiguous transaxial or coronal cines or a 3D SSFP sequence. Baffle-leaks may not be easy to identify by CMR, the suture line being long and tortuous. The measurement of pulmonary relative to aortic flow (Qp:Qs) may be useful, and any incompetence of the tricuspid valve into the systemic RV needs to be evaluated.
Cardiovascular magnetic resonance allows assessment of any RVOT or supravalvar PA stenosis, branch PA stenosis, the neo-AoV, and biventricular function.5 Previous myocardial infarction or fibrosis can be identified by LGE imaging, and assessment of the patency of the re-implanted coronary arteries and LV perfusion during pharmacological stress may be attempted by CMR.88
Cardiovascular magnetic resonance allows the assessment of possible stenosis or incompetence of the RV-to-PA conduit, the left ventricular outflow tract, of biventricular function, and possible residual shunt.
This malformation consists of discordant atrio-ventricular and discordant ventriculo-arterial connections. If uncomplicated, the affected patients can occasionally remain symptom free and undiagnozed into adulthood. Associated lesions include dextrocardia, a VSD, (sub-)pulmonary stenosis and Ebstein-like malformation of the left-sided tricuspid valve. The sub-aortic RV is prone to dysfunction and regurgitation of its tricuspid valve.89 Which ventricle is morphologically ‘right’ and which is ‘left’ can be determined from CMR short-axis and four-chamber cines, which show multiple coarse trabeculations, including the moderator band, arising from RV but not the LV side of the septum. Each atrio-ventricular valve and ventriculo-arterial connection should be visualized by appropriately aligned cines. Possible shunting through a VSD should be quantified, and the presence and severity of any (sub-)pulmonary stenosis or tricuspid regurgitation assessed.
Fontan operations, generally performed in children with only one effective ventricle, result in a fundamental departure from normal circulatory dynamics.6 The systemic and pulmonary vascular beds are connected in series downstream of the ventricle, so eliminating shunting at the cost of a critically elevated systemic venous pressure that maintains flow through the lungs. Earlier procedures incorporated the right atrium between the caval veins and pulmonary arteries, whereas total cavo-pulmonary connection, connecting inferior vena cave flow to the PAs via a lateral tunnel or extracardiac conduit, has been favoured in recent years.5 Cardiovascular magnetic resonance allows careful assessment of the Fontan cavo-pulmonary connections, branch pulmonary arteries, pulmonary veins (which can be compressed by the dilated right atrium of an atrio-pulmonary connection), the ventricle(s), the atrio-ventricular valve(s), the ventricular outflow tract, and any residual leaks or collateral vessels, although artefacts from ferromagnetic occlusion devices, as seen in some older patients, can preclude satisfactory CMR.90 Comprehensive coverage using a contiguous stack of transaxial cines is recommended, this generally being suitable for the identification of any intra-atrial thrombus or stenosis of the cavo-pulmonary connections. Velocity mapping can be used to assess flow through a suspected cavo-pulmonary narrowing where a peak jet velocity exceeding 1 m/s is likely to represent significant stenosis, and possible shunt flow through aorto-pulmonary collaterals.91 Should contrast injection for angiography be considered, the timing and distribution of contrast arrival in the PAs and its dilution by non-opacified (inferior) caval flow need to be borne in mind. Non-contrast 3D SSFP imaging, or injection of contrast from a leg, may be preferable. Evaluation of myocardial fibrosis by LGE may be informative in patients with impaired ventricular function.
Cardiovascular magnetic resonance allows clarification of anatomy and function, including anomalous vessels, connections, shunts, stenoses, abdominal situs, and possible polysplenia. Comprehensive cardiac, mediastinal, and upper abdominal coverage using stacks of contiguous transaxial and coronal cines is recommended. Dynamic contrast enhanced angiography and 3D SSFP are also useful. Cine images should be aligned with each inflow and outflow valve, and with any shunt flow, so that connections can be established. Cardiovascular connections are best described according to sequential segmental analysis.92,93 The relative pre-branch lengths of the left- and right-sided bronchi in coronal slices can provide a useful guide to thoracic situs, if in doubt. To distinguish a morphologically right from a LV, useful signs include the presence of a moderator band and additional coarse trabeculations arising from the RV side of the inter-ventricular septum, but not from its relatively smooth LV side.
The origin and proximal course of the coronary arteries can, in most patients, be visualized by CMR using cardiac gated 3D SSFP angiography, with fat suppression and without contrast agent.94,95 Either diaphragm navigator or breath-hold acquisitions are used to minimize respiratory blurring. Acquisitions may be repeated in different orientations if necessary. Image quality is dependent on meticulous acquisition technique. However, contrast enhanced multi-detector CT angiography generally gives clearer, more extensive depiction of the coronary arteries.
In addition to patients subject to myocardial ischaemia secondary to Kawasaki disease or with surgically re-implanted coronaries, acquired atheromatous disease is becoming increasingly important as patients with CHD become older. Computed tomography angiography is superior to CMR for coronary luminography but, without radiation hazard, CMR can give important information on global and regional myocardial function, viability, and perfusion.96,97
After transthoracic echocardiography, which remains the first-line imaging modality in ACHD, the choice of further imaging depends on the clinical questions that remain to be addressed. Besides tissue characterization, the strengths of CMR include comprehensive access and coverage, for example by the use of a stack of transaxial cine images or by dynamic contrast enhanced angiography, and the relatively accurate measurements of biventricular function and volume flow. These are particularly useful in the assessment and follow-up of adults after repairs of ToF, aortic coarctation, and transposition of the great arteries and those with Fontan operations or with operated or unoperated complex malformations. In the authors’ view, a dedicated CMR service should be regarded as a necessary facility of a centre specializing in the care of ACHD, and adults who were born with relatively complex CHD should ideally be investigated as well as managed in such a centre. To realize its full potential and to avoid pitfalls, however, CMR of CHD requires appropriate training and experience.
P.J.K. is supported by the British Heart Foundation. Funding to pay the Open Access publication charges for this article was provided by the CMR and GUCH Working Groups of the European Society of Cardiology.
Conflict of interest: none declared.
We would like to thank Helmut Baumgartner, Folkert Meijboom, other members of the GUCH and CMR Working Groups of the ESC for their contributions during preparation of the manuscript.