Pediatr Radiol (2015) 45:20–26 DOI 10.1007/s00247-014-3175-x

MINISYMPOSIUM

Cardiac magnetic resonance imaging in children Willem A. Helbing & Mohamed Ouhlous

Received: 13 March 2014 / Revised: 30 June 2014 / Accepted: 22 August 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract MRI is an important additional tool in the diagnostic work-up of children with congenital heart disease. This review aims to summarise the role MRI has in this patient population. Echocardiography remains the main diagnostic tool in congenital heart disease. In specific situations, MRI is used for anatomical imaging of congenital heart disease. This includes detailed assessment of intracardiac anatomy with 2-D and 3-D sequences. MRI is particularly useful for assessment of retrosternal structures in the heart and for imaging large vessel anatomy. Functional assessment includes assessment of ventricular function using 2-D cine techniques. Of particular interest in congenital heart disease is assessment of right and single ventricular function. Two-dimensional and newer 3-D techniques to quantify flow in these patients are or will soon become an integral part of quantification of shunt size, valve function and complex flow patterns in large vessels. More advanced uses of MRI include imaging of cardiovascular function during stress and tissue characterisation of the myocardium. Techniques used for this purpose need further validation before they can become part of the daily routine of MRI assessment of congenital heart disease.

Keywords Congenital heart disease . Magnetic resonance imaging . Phase-contrast magnetic resonance imaging . Ventricular function . Child W. A. Helbing : M. Ouhlous Department of Radiology, Erasmus Medical Centre — Sophia Children’s Hospital, Rotterdam, The Netherlands W. A. Helbing (*) Department of Paediatrics (Division of Cardiology), Sp-2.429, P.O. Box 2060, 3000, CB Rotterdam, The Netherlands e-mail: [email protected]

Introduction Congenital heart disease is the most common type of congenital malformations [1]. As a result of spectacular improvements in survival of these patients, the population with congenital heart disease is rapidly growing [2, 3]. This has resulted in an increasing need for diagnostic and interventional procedures that require imaging of the heart. Echocardiography remains the most commonly used tool for this purpose. However, other techniques with additional value over echocardiography, particularly MRI, and, to a lesser extent, CT angiography (CTA), are increasingly used. This is relevant in areas where echocardiography has important limitations, such as imaging of thoracic vessels, retrosternal structures, 3-D assessment of cardiac size and function and flow quantification. Another reason to use these techniques may be that they provide most of the required information within a single examination. In children, the lack of ionising radiation makes MRI the preferred technique in many situations [4]. The purpose of this condensed review is to provide a brief overview of current indications and practical protocols for MRI in congenital heart disease.

Cardiac MRI for congenital heart disease Cardiac MRI in congenital heart disease can be used for both anatomical as well as functional cardiac assessment. Recently international experts’ consensus reports on clinical indications and technical requirements have been published [5, 6].

Anatomical assessment Any anatomical assessment of congenital heart disease, with MRI or any other technique, should provide characterisation

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of the type of congenital heart disease according to the system of sequential segmental analysis [7]. This requires the assessment of the sidedness of the heart (levo- or dextrocardia), the situs (normal, inverse or ambiguous), the nature of atrioventricular connections (normal [concordant], discordant, absent, double-inlet) and ventriculoarterial connections (normal [concordant], discordant, single [absent], double-outlet) as well as the presence of additional malformations [7]. As a detailed description of this system is beyond the scope of this paper, the reader is referred to available literature for this purpose. Detailed assessment of intracardiac anatomy can be obtained with echocardiography in most infants and children with congenital heart disease. MRI and CT can be used if the acoustic window is insufficient, in case of complex anatomy of (partly) retrosternal structures or to image thoracic vessels. Because of radiation issues, MRI is the preferred technique in these situations. However, in young children, the use of MRI will require general anaesthesia because of relatively long scan times. CTA may be an acceptable alternative in those situations. In older children and adults, MRI is the preferred technique if echocardiography does not provide sufficient information. Anatomical assessment is mandatory before any invasive procedure, regardless of age. Since these procedures, surgical or by catheter intervention, are generally done at a young age (infants, young children), anatomical imaging of congenital heart disease is particularly important in these age groups. However, during follow-up, anatomical imaging continues to be important. For identification of anatomy according to the system of sequential segmental analysis, MRI is an excellent technique. To study the anatomy of the atria, the anatomy of the atrial appendages needs to be identified. The anatomy of the ventricles can be recognised by their respective landmarks. For

the left ventricle, these are the presence of a mitral valve, fibrous continuity between atrioventricular valve and semilunar valve (if connected to the left ventricle) and a relatively smooth trabecular surface. Landmarks of right ventricular anatomy are the presence of a subarterial infundibulum, heavy trabeculation in the apical part, trabecula septomarginalis and a tricuspid valve (if present). Two-dimensional and 3-D techniques may be used for anatomical assessment. Two-dimensional techniques include widely available sequences such as black-blood fast spin-echo (FSE) and balanced steady-state free precession (SSFP) sequences, which may be obtained in standard axial, coronal and sagittal planes as well as in double-oblique orientations, tailored to the specific situation. Three-dimensional techniques include contrast-enhanced MR angiography and (isotropic) 3-D SSFP [8, 9]. These sequences may be used to obtain images with adequate spatial resolution to provide useful 3-D reformatting and segmentation for anatomical diagnosis. In clinical practice, these techniques have been used extensively. Figures 1, 2, 3 and 4 provide examples of different techniques used in different lesions. Common indications for anatomical assessment with MRI in congenital heart disease are

Fig. 1 a MRI of a 10 year old boy with a normal heart. Steady state free precession sequence was used, in 4-chamber orientation. Note offset of mitral and tricuspid valve (arrow) b MRI of 33 year old female patient with congenitally corrected transposition of the great arteries. Steady state free precession sequence was used, in 4-chamber orientation. Note offset

of mitral and tricuspid valve (arrow), which differs from that in normal heart. Also note atrioventricular discordance and flow artefact at central part of closed tricuspid valve, representing tricuspid regurgitation. LA left atrium; LV left ventricle; RA right atrium; RV right ventricle; * mitral valve; # tricuspid valve

& & & &

abnormalities of the aortic arch (coarctation, interruption, double arch, common arterial trunk, vascular slings), pulmonary arteries (aorta-to-pulmonary collaterals, pulmonary sling, peripheral pulmonary stenosis), anatomy of the pulmonary veins, including anomalous pulmonary venous drainage, pulmonary vein stenosis, often post-intervention and intracardiac baffles, such as may be present after atrial redirection procedures for transposition of the great

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Fig. 2 MRI in a 12 year old boy who had been operated on for coarctation of the aorta in early childhood. Black-blood fast spinecho double oblique (a) and steady-state free precession (b) MRI of the aortic arch. Note recurrent coarctation (arrow) of the aorta (Ao)

&

arteries (Mustard and Senning operation) or the Fontan procedure for univentricular hearts, venovenous collaterals [10–15].

Table 1 provides a summary of preferred tomographic imaging technique and of MRI sequences recommended for anatomical and/or functional evaluation of the most common types of congenital heart disease. The reader is also referred to

Fig. 3 3D reconstruction of contrast enhanced MR angiogram in 8-year old-boy with pulmonary atresia with intact ventricular septum, s/p surgical pulmonary valvotomy and modified Blalock-Taussig shunt (arrow) from right subclavian artery to right pulmonary artery

Fig. 4 Steady-state free precession MRI in the sagittal orientation in a 34-year-old man with transposition of the great arteries treated with the Mustard operation. In this operation, the inferior and superior vena cava are redirected to the left ventricle, the pulmonary veins are redirected to the right ventricle. This restores the normal circulatory pattern (oxygen-poor blood enters the pulmonary circulation, oxygen-rich blood enters the systemic circulation; the right ventricle is the ventricle supporting the systemic circulation). These patients may develop narrowing of the connection (baffle) of the caval veins to the left ventricle or of the connection of the pulmonary veins to the right ventricle. The patient in the image has narrowing of the connection (arrow) of the superior vena cava to the right ventricle. RV right ventricle, Ao aorta, $ inferior vena cava

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Table 1 Summary of preferred tomographic imaging technique and of MRI sequences recommended for anatomical and/or functional evaluation of the most common types of congenital heart disease. See also two

recent, more extensive overviews on the subjects by Fratz et al. [5] and by Valsangiacomo Buechel et al. [6]

Preferred tomographic Recommended MR sequence imaging modality in adjunct to echocardiography

Aortic arch anomaly MRI or CT Cardiomyopathies MRI Complex congenital heart disease Infants: CT Follow-up: MRI Pulmonary arteries MRI or CT Pulmonary veins MRI or CT Shunt lesions MRI Single ventricles Infants: CT Follow-up: MRI Tetralogy of Fallot MRI

2-D SSFP 3-D contrast-enhances MR angiography b a a a b

Phase-contrast flow Black-blood LGE fast spin-echo b c b c b a c

c c b a

a a b b

b c a a

c c c c

b

a

b

a

c

b

LGE late gadolinium enhancement, SSFP steady state free precession a Essential technique for anatomical characterisation / functional quantification in this lesion b Useful technique, commonly applied in assessment of anatomy or (ventricular) function of the lesion c Helpful technique. In many instances, echocardiography may provide similar information provided there is an adequate acoustic window

recent overviews on these subjects by Fratz et al. [5] and Valsangiacomo Buechel et al. [6].

Functional assessment With the aging of the congenital heart disease population, the risk of heart failure has increased considerably. Heart failure in these patients has been associated with residual lesions after corrective surgery, such as residual valve regurgitation and/or stenosis, situations in which the right ventricle supports the systemic circulation, univentricular hearts and pulmonary hypertension. Among the patients with highest risk for heart failure after surgery for congenital heart disease are those who have been operated for tetralogy of Fallot, transposition of the great arteries (Mustard/Senning operations) and patients who have had the Fontan operation [16]. In these situations, repeated assessment of the function of the left and right ventricles or single ventricle is required during follow-up. Quantification of residual shunts and/or valvular lesions may also be important in the follow-up of these patient groups. MRI is a particularly useful technique for these purposes. Firstly, MRI provides an unobstructed and intrinsically 3-D view of the heart, which is particularly useful for quantification of right ventricle and single ventricular function. The right ventricle is located behind the sternum, which is a problem for echocardiography. The shape of the right ventricle is complex and may vary considerably in congenital heart disease [17, 18]. Univentricular hearts are a heterogeneous group of lesions, both from the perspective of anatomy as well as from the point

of view of geometry of the ventricle. This makes it unattractive to assess cardiac chamber dimensions with echocardiography in patients with right or single ventricular lesions. Secondly, in various situations with haemodynamic relevance, quantification of flow through valves and/or large vessels contributes to clinical assessment. Phase-contract MRI has been validated as a useful technique to quantify flow. In contrast to echocardiography, phase-contrast MRI may provide quantification of actual flow volume, which may be very useful in different situations [19–23]. Quantification of ventricular size and function is commonly done with cine-SSFP sequences. Care is taken to include the entire ventricles throughout the cardiac cycle. Generally, 8–12 slices with a thickness of 6–10 mm are used for this purpose. Temporal resolution is an important aspect of these cine series, and should not be below 24 phases/cardiac cycle in order to be able to adequately delineate the moment of end-systole. Normal data sets have been available for adults and children [24–27]. Please note that differences in contouring techniques, genetic background and activity levels in the reference population and differences in statistical modelling may result in different normal ranges. In adult cardiology, it is common to acquire cine images of the contracting ventricles aligned with the left ventricular short axis. This orientation is widely used in congenital heart disease as well and has adequate reproducibility and observer variability [28]. Sources of inaccuracy include endocardial border detection, slice thickness/partial volume effects, motion effects and problems in delineation of atrioventricular, ventriculoarterial and semilunar valves in the left ventricular short axis orientation. It has been advocated that the latter

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problem may be easier to deal with in axial orientation or right ventricular outflow tract oriented images [29, 30]. Functional assessment is mandatory before any invasive procedure, regardless of age. In most instances, this can be done semiquantitatively with echocardiography, particularly in infants and young children. After repeat interventions, in case of residual haemodynamic abnormalities and with increasing age, accurate quantification of ventricular size and function becomes increasingly important. MRI is commonly used for this purpose, in addition to echocardiography. Functional assessment may include flow quantification. Phase-contrast MRI with encoded velocity has obtained an important role in the assessment of congenital heart disease. The reason for this is the unique capability to assess flow volume across a vessel of interest with this technique. To assess flow volume, a slice is placed perpendicular to the vessel or valve of interest. After contouring this vessel/valve, the volume of blood passing through the plane is calculated as the product of flow velocity and cross-sectional area. In congenital heart disease, phase-contrast MRI has been used to quantify the size of intra- and extracardiac shunts [19, 21, 32] and the extent of valvular regurgitation and stenosis [22]. Another common application is assessment of flow through intracardiac baffles, such as in the Fontan operation. Common pitfalls include misalignment with flow, turbulent flow, malpositioning with regard to valve plane, through plane motion, effects of breathing, effects of eddy currents and other artefacts, and incorrect setting of velocity encoding [33, 34]. Figures 5, 6 and 7 provide examples of common indications and use of phase-contrast MRI. A promising new development is imaging of flow in the heart and large vessels in 4-D [35]. This has been a research tool that has led to increased insight in intracardiac and large vessel flow patterns and that may be relevant for long-term outcome. Currently, assessment of 4-D flow has not been incorporated in clinical workflow in most institutions. This may rapidly change as soon as quantification of 4-D flow will become a practical possibility [36].

Fig. 5 Phase-contrast MRI to assess through plane flow at the level of the mitral valve. a Modulus image. b Phase-contrast image to assess throughplane flow at the level of the mitral valve (MV). c After assessment of the area of the mitral valve, flow velocity per cardiac phase can be plotted

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Fig. 6 Flow curves of flow across the main pulmonary artery and aorta in a patient with intracardiac left to right shunt at atrial level. Pulmonary artery flow is 2.5 times higher than aortic flow, indicating a left to right shunt ratio of 2.5 to 1. Ao aorta, PA pulmonary artery [31].

Table 1 provides a summary of preferred tomographic imaging technique and of MRI sequences recommended for anatomical and/or functional evaluation of the most common types of congenital heart disease. The reader is also referred to recent overviews on these subjects by Fratz et al. [5] and Valsangiacomo Buechel et al. [6].

Advanced functional assessment In congenital heart disease, there is a strong need for tools that help in assessment of long-term risk for patients, particularly the changes of developing heart failure. Assessment of regional ventricular function and detailed assessment of atrial and diastolic ventricular function may contribute to risk assessment [37, 38]. Commonly, assessment of cardiac function is done at rest, which seems a poor way of testing the function of the heart. In analogy to the situation in acquired adult heart disease, several centres have used stress MRI to evaluate flow and function of the heart and great vessels in congenital heart disease [39]. Stress can be either physical or pharmacological [39]. Reported experience suggests that both types of stress can be used safely in children with congenital heart disease [39]. Since hard endpoints

against time in the cardiac cycle. This provides the typical mitral valve inflow pattern, with early and late diastolic flow volume peaks, corresponding to filling after ventricular relaxation during early diastole and late filling after atrial contraction

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Fig. 7 Phase-contrast MRI. a To assess through plane flow in the main pulmonary artery in a 17 year old female patient operated for tetralogy of Fallot, with residual pulmonary regurgitation. In this figure, phasecontrast MRI of flow in the pulmonary artery overlay the flow versus time curve. b Flow direction changes from antegrade from the right

ventricle into the pulmonary artery in systole (first 3 flow images, read from left to right) to retrograde flow from the pulmonary artery into the right ventricle during diastole (last 2 images, read from left to right). With changes in flow direction and velocity the grey value of the pixels in the area of interest change accordingly

like death, hospitalisation and re-interventions are relatively scarce in congenital heart disease, it is difficult to prove the prognostic value of this type of imaging. However, recent work suggests that low-dose dobutamine stress MRI may be useful to assist in decision-making in patients with systemic right ventricles and tetralogy of Fallot [40, 41]. Tissue characterisation may have an important role in congenital heart disease. For this purpose, myocardial scar imaging with late gadolinium enhancement is a widely used technique that has demonstrated prognostic value in the adult congenital heart population. Imaging of diffuse myocardial fibrosis may be very attractive in this population. In addition, tissue characterisation using T1-mapping sequences has become an interesting field for researchers. Late gadolinium enhancement is excellent in demonstrating localised areas of infarct and scar tissue. However, late gadolinium enhancement is not able to depict more diffuse disease. Factors like pressure overload, volume overload, aging, oxidative stress and activation of the sympathetic and renin-angiotensinaldosterone system may cause an increase in collagen content in myocardial volume [42]. This may lead to interstitial myocardial fibrosis. By directly quantifying T1 values for each voxel in the myocardium, a parametric map can be generated representing the T1 relaxation times of any region of the heart without the need to compare it to a normal reference standard before or after the use of a contrast agent. The modified look-locker inversion-recovery (MOLLI) technique is the most widely used T1-mapping sequence. This sequence was first described by Messroghli et al. [43]. The sequence consists of a single-shot TrueFISP image with acquisitions over different inversion time readouts allowing for magnetisation recovery of a few seconds after 3 to 5 readouts. The advantage of this sequence is the relatively short breath-hold, high spatial resolution (1.6 × 2.3 × 8 mm) and sufficient dynamic signal. T1 mapping can be used to assess any disease that affects the myocardium. However, none of the techniques currently

used for this purpose has been fully established in congenital heart disease, particularly not in children. Conclusion MRI has become a very important additional imaging tool in the clinical management of congenital heart disease. Its main strengths are anatomical imaging, which is of particular importance in the large vessels, for retrosternal structures (and in patients with poor acoustic windows). For functional imaging, intrinsically 3-D assessment of the size and function of heart chambers with complex geometry, such as the right ventricle and single ventricles is an established reference technique. Velocity-encoded MRI has various indications on congenital heart disease, particularly in the assessment of intracardiac shunt size and quantification of valve regurgitation.

Conflicts of interest None

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Cardiac magnetic resonance imaging in children.

MRI is an important additional tool in the diagnostic work-up of children with congenital heart disease. This review aims to summarise the role MRI ha...
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