Utility of late gadolinium enhancement in pediatric cardiac MRI

Transcription

1 Pediatr Radiol (2016) 46: DOI /s REVIEW Utility of late gadolinium enhancement in pediatric cardiac MRI Maryam Etesami 1 & Robert C. Gilkeson 1 & Prabhakar Rajiah 1 Received: 10 August 2015 /Revised: 22 October 2015 /Accepted: 26 November 2015 /Published online: 30 December 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract Late gadolinium enhancement (LGE) cardiac magnetic resonance (MR) imaging sequence is increasingly used in the evaluation of pediatric cardiovascular disorders, and although LGE might be a normal feature at the sites of previous surgeries, it is pathologically seen as a result of extracellular space expansion, either from acute cell damage or chronic scarring or fibrosis. LGE is broadly divided into ischemic and non-ischemic patterns. LGE caused by myocardial infarction occurs in a vascular distribution and always involves the subendocardial portion, progressively involving the outer regions in a waveform pattern. Non-ischemic cardiomyopathies can have a mid-myocardial (either linear or patchy), subepicardial or diffuse subendocardial distribution. Idiopathic dilated cardiomyopathy can have a linear mid-myocardial pattern, while hypertrophic cardiomyopathy can have fine, patchy enhancement in hypertrophied and non-hypertrophied segments as well as right ventricular insertion points. Myocarditis and sarcoidosis have a mid-myocardial or subepicardial pattern of LGE. Fabry disease typically affects the basal inferolateral segment while Danon disease typically spares the septum. Pericarditis is characterized by diffuse or focal pericardial thickening and enhancement. Thrombus, the most common non-neoplastic cardiac mass, is characterized by absence of enhancement in all sequences, while neoplastic masses show at least some contrast enhancement, depending on the pathology. Regardless of the etiology, presence of LGE is * Prabhakar Rajiah radprabhakar@gmail.com 1 Cardiothoracic Imaging, Department of Radiology, Case Western Reserve University School of Medicine, University Hospitals Case Medical Center, Euclid Ave., Cleveland, OH 44106, USA associated with a poor prognosis. In this review, we describe the technical modifications required for performing LGE cardiac MR sequence in children, review and illustrate the patterns of LGE in children, and discuss their clinical significance. Keywords Children. Gadolinium. Heart. Late gadolinium enhancement. Magnetic resonance imaging. Myocardium Introduction Cardiac MRI has become an integral part of the evaluation of cardiovascular disorders in children. Cardiac MR is valuable not only in the evaluation of complex cardiac anatomy but also in quantification of ventricular and valvular function. Late gadolinium enhancement (LGE) imaging is an important sequence used in cardiac MR. The principle of this sequence is that gadolinium-based contrast agents wash in and out of normal myocardium rapidly, but they wash in abnormal tissues such as scar/fibrosis slowly and have prolonged retention. The prolonged contrast retention causing LGE is from increased distribution of contrast agent into extracellular space, where it gets trapped. In acute conditions (such as acute myocarditis or acute myocardial infarction), increased volume of contrast distribution into extracellular space results from cellular injury or damage. In chronic conditions (such as scar of chronic myocardial infarction or fibrosis in cardiomyopathies), the extracellular space is expanded and retains more contrast agent. In this article we discuss the technique of LGE, technical modifications required in children and different causes of LGE in children (Table 1), and we illustrate these disease processes (Fig. 1). We also review the literature on the current evidence for the clinical significance of the presence of LGE in several etiologies.

2 Pediatr Radiol (2016) 46: Table 1 Causes of late gadolinium enhancement in children Category Diseases LGE pattern LGE location Post-surgical expected Post-surgical more than normally expected Myocardial infarction Patch repair of VSD Tetralogy of Fallot repair Septal ablation of HCM Ablation of arrhythmogenic focus Coronary artery injury/surgeries Tetralogy of Fallot D transposition Transmural RV wall Transmural Transmural Subendocardial/transmural Full thickness Full-thickness/small foci in Patch site RVOT at surgical site Ablation site Ablation site Vascular distribution Beyond RVOT surgical site Anterior RV/basal septal trabeculations/rv insertion points Fontan shunt Variable (most common: transmural) Variable (most common: primary ventricle free wall) Kawasaki disease Anomalous coronary arteries Coronary artery dissection Coronary fistula Myocardial bridge Aortic stenosis Always involves the subendocardial portion and extends variably toward epicardium Transmural in severe infarct Cardiomyopathies Idiopathic dilated cardiomyopathy No LGE (most common)/ mid-myocardial Storage disorders In a vascular distribution Ventricular septum HCM Mid-myocardial Hypertrophied muscle/ RV insertion ARVD/C RV wall RV: sub-tricuspid portion/ outflow tract/mid-free wall Left ventricular non-compaction Variable (most common: mid-myocardial) LV Sarcoidosis Subepicardial/mid-myocardial Variable Anderson Fabry disease Danon disease Muscular dystrophy Duchenne dystrophy Becker dystrophy Inflammatory Myocarditis Pericarditis Masses non-neoplastic Thrombus No LGE Benign neoplasms Rhabdomyoma Fibroma Myxoma Malignant neoplasms Metastasis Leukemia/lymphoma Sarcoma Mid-myocardial/sub-epicardial Subendocardial/mid-myocardial/ transmural Subepicardial Mid-myocardial or subepicardial Pericardial No LGE Heterogeneous Heterogeneous Variable Diffuse heterogeneous, variable in nodules Heterogeneous Basal inferolateral wall Relative sparing of ventricular septum Mostly in the free wall Variable Pericardium ARVD/C arrhythmogenic right ventricular dysplasia/cardiomyopathy, HCM hypertrophic cardiomyopathy, LGE late gadolinium enhancement, LV left ventricle, RV right ventricle, RVOT right ventricular outflow tract, VSD ventricular septal defect Technique of late gadolinium enhancement in children LGE imaging is performed min following intravenous administration of mmol/kg of gadolinium-based contrast agent. A recent paper showed variability in the use of contrast agent across institutions [1]. At our institution we use 0.2 mmol/kg when estimated glomerular filtration rate (egfr) is >60 ml/min/1.73 m 2 and 0.1 mmol/kg when egfr is ml/min/1.73 m 2. Because of the risk of nephrogenic systemic fibrosis, the use of gadolinium-based contrast agent should be avoided in acute renal disease or chronic disease with egfr<30 ml/min/1.73 m 2. Caution should also be exercised in preterm neonates and infants because of renal immaturity and potential egfr<30 ml/min/1.73 m 2 [1, 2]. A 180 inversion pulse is applied and images are acquired when the normal myocardium has relaxed and has reached the zero point, where it has no signal. The sequence is electrocardiography-gated and images are acquired in mid to late diastole to minimize cardiac motion. Selecting the optimal inversion time (TI) is critical because artifactual high signal can be seen both at low and high TIs. The optimal TI is determined by performing a T1 scout sequence, which rapidly acquires multiple low-resolution LGE images at different TIs. The

3 1098 Pediatr Radiol (2016) 46: performed with free-breathing technique using navigator gating of diaphragmatic motion [4]. Technical modifications Fig. 1 Patterns of late gadolinium enhancement in children. a Infarcts always involve the subendocardium, progressively extend to the subepicardium to varying degrees and can be full-thickness transmural as demonstrated by different colors: light green subendocardial (<25%); dark green partial thickness (26 50%); blue near full thickness (51 75%); orange full thickness (>75%). b Non-infarct patterns of enhancement include mid-myocardial (red), which is seen in myocarditis, sarcoidosis and Fabry disease; linear mid-myocardial (blue), which is seen in myocarditis, sarcoidosis and idiopathic dilated cardiomyopathy; subepicardial (green), which is seen in myocarditis, sarcoidosis and Fabry disease; fine interstitial (yellow), which is seen in hypertrophic cardiomyopathy; at right-ventricular insertion points (purple), seen in hypertrophic cardiomyopathy, pulmonary hypertension and systemic sclerosis; or diffuse subendocardial (teal), seen in endomyocardial fibrosis and amyloidosis, although amyloidosis is very rare in children normal TI varies from 260±30 milliseconds in a 1.5-tesla scanner to 330±49 msec in a 3-T scanner [3]. An alternative is to perform a phase-sensitive inversion recovery sequence, which is less sensitive to TI than the conventional inversion recovery sequence. In addition, it has higher contrast-to-noise ratio with lower background noise. LGE imaging can be performed either with a segmented gradient-echo (FLASH [fast low angle shot]) or steady-state free precession (SSFP) techniques, in either a 2D or 3-D mode. It is performed in a single breath-hold, over 9 12 heartbeats; in patients who cannot breath-hold it can be Cardiac MR is challenging in children because of several factors including the small body size with small size of cardiac structures, rapid heart rates and non-compliance with breathing instructions. Children younger than 7 years and even older children with cognitive impairment are scanned under general anesthesia to ensure reliable breath-holding for prolonged periods. This decision is made after discussion between the cardiac imager and the anesthesiologist following a risk benefit analysis. An adequately trained anesthetic team with MRcompatible monitoring equipment is necessary for safe administration of anesthesia. An efficient scan protocol tailored to answer the specific clinical question should be performed. In infants younger than 6 months, adequate sedation is often achieved with feed, swaddle and sleep technique [5]. With small children, a high in-plane spatial resolution of up to mm is required. To obtain this, a small field of view along with larger matrix is used. The slice thickness is also reduced to 3 5 mm. The small field of view and thin slice thickness result in lower signal-to-noise ratio (SNR). A small multi-element pediatric cardiac phased-array coil is used to obtain high SNR. Use of two signal averages improves the SNR but results in longer acquisition time. Parallel imaging is used to accelerate image acquisition, but it decreases SNR [6 8]. A high temporal resolution (20 60 msec) is also required because of children s high heart rates (up to 150 beats per minute). To achieve this, the number of k-space lines (views per segment) acquired in each R-R interval is adjusted to the heart rate [7]. This is even more challenging in children with arrhythmia. Inversion-recovery LGE sequences are typically obtained with inversions every two R-R intervals to allow for longitudinal signal recovery between successive inversion pulses and to avoid signal loss. However at high heart rates (>100 bpm) triggering is performed every three R-R or even four R-R intervals. Also, at high heart rates the data acquisition (shot) duration should be decreased by decreasing the number of views (k-space lines) per segment (turbo factor) to reduce blurring from faster heart motion [5]. In children with arrhythmia, segmented inversion-recovery sequence results in motion artifact, hence a single-shot SSFP sequence can be used because a slice is obtained in one heartbeat, although this has slightly lower SNR than a segmented sequence [4]. Arrhythmia rejection is another method to reduce artifacts from arrhythmias. In poor breath-holders, single-shot acquisition or motion-corrected multiple-signal averaging or acquisition with navigator gating of the diaphragm is preferred. Table 2 summarizes the technical parameters for LGE imaging in children.

4 Pediatr Radiol (2016) 46: Table 2 Coil Image acceleration Contrast dose Acquisition ECG gating Breathing Sequence Planes Slice thickness In-plane spatial resolution Signal averaging Acquisition phase Triggering Turbo factor Late gadolinium enhancement technique in children Normal appearances Normal myocardium is completely nulled and appears dark on an LGE sequence, whereas blood pool has intermediate signal between the normal myocardium and scar. In addition, several artifacts may mimic LGE, such as partial volume averaging, contrast in recesses and contrast in the septal perforator coronary arterial branch. Post-surgical appearance Small pediatric multi-element phased-array coils Parallel imaging mmol/kg min after contrast administration Prospective ECG triggered/single-shot non-ecg-gated Breath-hold/free-breathing with respiratory/ navigator gating/signal averaging/ single-shot imaging 2-D or 3-D, conventional or PSIR, SSFP or FLASH Left ventricle- short axis, 2-chamber, 3-chamber, 4-chamber; Right ventricle- 2- chamber, outflow tract, horizontal long axis 3 5 mm mm Two Late diastole Every 2 nd,3 rd or 4 th heartbeat Appropriate to heart rate, shorter at higher heart rates ECG electrocardiogram, FLASH fast low-angle shot, PSIR phase-sensitive inversion recovery, SSFP single-shot fast spin echo LGE is normally expected at locations of surgeries that involve placement of fibrous tissues such as patches. This might be seen, for example, in the ventricular septum at the site of ventricular septal defect patch [9] and in the right ventricular outflow tract (RVOT) following tetralogy of Fallot repair and patch placement (Fig. 2) [10]. LGE is also seen following alcoholic septal ablation for hypertrophic cardiomyopathy (HCM) as a full-thickness transmural LGE in the basal ventricular septum. Occasionally extensive LGE is seen following surgeries for congenital cardiovascular diseases, and this is generally associated with adverse prognosis [11]. Scarring can also be an iatrogenic complication, especially in surgeries involving coronary arteries such as reimplantation or inadvertent injury of coronary arteries. In tetralogy of Fallot (TOF), cardiac MR is the reference standard for quantification of right ventricle size, right ventricle function and pulmonary regurgitation following repair. Some LGE is normally seen at the site of surgery in the right ventricular outflow tract, particularly following transannular patch repair (as described above), but occasionally it extends well beyond the surgical site (Fig. 2) and involves any of the right ventricular walls, most commonly the anterior wall [12]. Right ventricular LGE after tetralogy of Fallot repair depends on the postoperative follow-up time. The longer the follow-up time, the more common LGE is in the right ventricle [12, 13]. A greater degree of right ventricular LGE has been shown to be associated with increased RVOT diameter, increased RV end-diastolic volume, lower right ventricular ejection fraction, pulmonary regurgitation, arrhythmia and lower exercise capacity, all of which imply poor prognosis [10, 12, 14, 15]. LGE in the left ventricle has been reported variously in different studies, more commonly in adults (53%) [14] than inchildren(0%)[12]. Differences in left ventricular LGE could also be the result of different surgical eras with different approaches. LGE is seen in 61% of patients following atrial switch procedure for D-transposition of the great arteries. LGE can be seen because of myocardial fibrosis from either preoperative hypoxemia or from demand supply mismatch caused by increased myocardial mass or decreased myocardial flow reserve. Four patterns of enhancement are seen: localized fullthickness enhancement of anterior right ventricle (44%); small foci in trabeculations (44%); basal septal enhancement (19%); and enhancement at right ventricular insertion points (superior 36%, inferior 89%). The extent of LGE has been shown to correlate with age, right ventricle dysfunction, QRS duration, QT dispersion and clinical events (arrhythmia and sudden cardiac death), all of which imply adverse prognosis [16]. LGE has been seen in 28% of patients who had Fontan operation. The most common location of LGE after a Fontan operation is the free wall of the primary ventricle (64%), and less common locations include the free wall of the secondary ventricle, ventricular septum, apex, papillary muscles and surgical sites. The pattern of enhancement is also variable, including transmural (40%), subendocardial (32%), subepicardial (20%), endocardial fibroelastosis (16%) and speckled (12%). Presence and extent of LGE correlate with lower ejection fraction, dilated and hypertrophied systemic ventricle, regional wall motion abnormalities and nonsustained ventricular tachycardia [17]; however positive LGE is shown not to be associated with clinical endpoints (i.e. death or listing for cardiac transplant) [18]. Myocardial infarction Myocardial infarction is less common in children than adults. It is caused by coronary vasculitis, Kawasaki disease,

5 1100 Pediatr Radiol (2016) 46: Fig. 2 Post-surgical patterns of late gadolinium enhancement. a Fourchamber steady-state free precession (SSFP) late gadolinium enhancement (LGE) cardiac MR image in a 12-year-old girl shows LGE (arrow) in the basal membranous portion of the ventricular septum, at the site of a VSD patch placed as part of surgical repair of tetralogy of Fallot. b Short-axis SSFP LGE cardiac MR image in a 17- year-old boy with tetralogy of Fallot repaired by transannular patch shows normally expected LGE (arrows) limited to surgical site in the right ventricular outflow tract (RVOT). c Short-axis SSFP LGE image in a 14-year-old girl with tetralogy of Fallot repaired by transannular patch shows extensive scarring (arrows) of the RVOT extending inferiorly into the free wall and the septum, well beyond the expected surgical site. There is also aneurysmal dilation of the RVOT. LV left ventricle, RV right ventricle, VSD ventricular septal defect anomalous coronary arteries, myocardial bridging, congenital hypercholesterolemia, coronary artery fistula, coronary dissection and embolus. Clinical findings are chest pain, dyspnea, palpitation, syncope, poor cardiac output and dizziness. Cardiac MR has an important role in the evaluation of myocardial infarction. Cardiac MR demonstrates wall motion abnormalities on cine steady-state free precession (SSFP) images as well as edema of acute infarction as high signal on T2- weighted images in myocardium of the affected vascular territory. This area of edema in MRI performed 2 days after infarct enables retrospective identification of the area at risk, which is defined as the hypoperfused myocardium at the time of ischemia. Cardiac MR is also useful in establishing the etiology of myocardial infarction, including evaluation of coronary arteries. Coronary MR angiography can be performed using a navigator-gated 3-D SSFP sequence [19]or inversionrecovery fast low-angle shot (IR-FLASH) sequence following injection of blood-pool contrast [20], either with a whole-heart or a targeted approach. The advantage of cardiac MR is the absence of ionizing radiation, but disadvantages include long scanning time, lower spatial resolution and operator dependency. Coronary MR angiography is appropriate for the evaluation of coronary artery anomalies, particularly those involving the origin [19, 21], fistulas, ectasias, aneurysms and bypass grafts [22]. However, coronary MR angiography is still not ideal or appropriate for evaluation of coronary artery stenosis [23]. Recent advances with the use of high-field magnets, multi-channel coils and software developments might improve results. LGE sequence is useful in establishing the diagnosis of MI in children, particularly when the presentation is atypical. LGE in a myocardial infarct always involves the subendocardial portion and extends to variable extent toward the epicardium and is transmural in a severe infarct (Fig. 1). LGE in acute MI is caused by damaged cell membranes that result in intracellular space becoming extracellular; in chronic myocardial infarction, LGE is caused by the presence of scar that results in expansion of extracellular space [24]. LGE cardiac MR can also quantify the scar. In a qualitative technique, the scar in each of the 17 myocardial segments is scored on a 5-point scale: 0=no enhancement, 1=<25% enhancement of the myocardial thickness, 2=26 50%; 3=51 75%; 4>75% enhancement (Fig. 1). A total score can be obtained by summing the scores of all segments and dividing by 17. This quantification of scar by LGE is useful in the evaluation of myocardial viability for coronary revascularization procedures because there is an inverse correlation between the extent of scar and recovery of contractile function [25]. Cardiac MR can also detect various complications of MI such as free wall rupture, ventricular septal rupture, aneurysm/ pseudoaneurysm, pericardial effusion/pericarditis, thrombus, mitral regurgitation, right ventricle infarction and cardiac failure [26]. We provide a brief description of the role of MRI in the evaluation of few of the etiologies of myocardial infarction. Kawasaki disease Kawasaki disease (also known as mucocutaneous lymph node syndrome) is an acute systemic vasculitis that predominantly occurs in young children. Cardiovascular manifestations especially coronary artery aneurysms are common and are the leading cause of long-term morbidity and mortality. Myocardial inflammation is very common during the acute phase, but it usually responds well to intravenous immunoglobulin (IVIG) without long-term fibrosis. IVIG also decreases the risk of coronary artery

6 Pediatr Radiol (2016) 46: aneurysms. Myocardial infarction can develop from slow blood flow or thrombosis within a coronary artery aneurysm (Fig. 3) or progression of aneurysms to stenosis. Cardiac MR is a valuable noninvasive method for simultaneous evaluation of coronary arteries, cardiac function, myocardial inflammation, infarction, and viability [27]. MR angiography enables noninvasive detection, quantification and follow-up of coronary artery aneurysms [28]. Late gadolinium enhancement MRI can detect myocarditis in the acute phase and myocardial infarction/fibrosis in follow-up imaging (Fig. 3). LGE is uncommon in longterm follow-up of children with Kawasaki disease, but when present LGE is associated with long-term left ventricular dysfunction [29]. Anomalous coronary arteries Anomalous coronary arteries have been detected in 0.5% of pediatric autopsies [30]. Anomalous origin of coronary artery from the opposite coronary sinus is the most common type of anomaly. An inter-arterial course of the coronary artery (between pulmonary artery and aorta) is associated with arrhythmia, ischemia and sudden cardiac death [30]. Additionally, longer intramural course of the anomalous coronary artery is correlated with more symptoms such as chest pain and syncope [31]. Cardiac MR is good in simultaneous detection of coronary artery anomalies, especially those involving the origins and proximal coronary arteries [19, 21], and any effects on the myocardium, such as ischemia or infarct. Coronary artery dissection Coronary artery dissection is uncommon in children. It can occur either spontaneously in the peri-partum period or with connective tissue disorders such as Marfan syndrome, Ehlers Danlos syndrome or Loeys Dietz syndrome. It can also be iatrogenic, caused by chest trauma, or an extension of aortic dissection. MR angiography can be used for evaluation of coronary arteries, but CT angiography has higher spatial resolution (Fig. 4). In addition, late gadolinium enhancement sequence can evaluate the myocardium for ischemia/ infarction (Fig. 4). Coronary fistula Coronary artery fistula is an abnormal termination of a coronary artery or its branches into one of the cardiac chambers or the great vessels adjacent to the heart, such as a pulmonary vessel. Coronary artery fistula is a rare abnormality, with the majority of cases being congenital. Most patients are asymptomatic and are incidentally diagnosed on cardiac imaging, but some present with chest pain, exertional dyspnea or fatigue [32]. The fistula may cause blood drainage from normal myocardium, known as myocardial steal phenomenon, resulting in myocardial ischemia, possibly infarction and arrhythmia [32, 33]. Cardiac MR can delineate the anatomy of the fistula and also detect and quantify infarcts (Fig. 5). Myocardial bridging Fig. 3 Kawasaki disease. a CT angiography in a 7-year-old girl with Kawasaki disease shows dilated left coronary artery (arrow). In addition, there is thrombosis of the proximal right coronary artery (arrowhead). b Short-axis SSFP LGE cardiac MR image in the same girl shows a full-thickness transmural infarct (arrow) ofthebasal inferoseptal and basal inferior segments, secondary to thrombosed right coronary artery aneurysm, shown in the previous image. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession Myocardial bridging is an intramyocardial course of an epicardial coronary artery and is most common in the middle segment of the left anterior descending coronary artery. The prevalence in the general population varies among studies, with a much higher rate at autopsy (up to 86%) compared to angiography (less than 5%) [34]. This difference could be a result of angiographic methods of diagnosis based on coronary compression during systole, which is not present in all

7 1102 Pediatr Radiol (2016) 46: Fig. 4 Coronary artery dissection. a Curved multiplanar reconstruction of a coronary CT angiogram following intravenous contrast administration in a 10-year-old boy shows a subtle dissection flap with thrombosed false lumen of the mid left anterior descending coronary artery (arrows). b Short-axis SSFP LGE cardiac MR image in the same boy shows near-full-thickness transmural enhancement in the apical inferior segment (arrows), consistent with an infarct in the distal left anterior descending artery territory. T2-weighted MR image (not shown) showed myocardial edema, indicating acute myocardial infarction. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession cases. There are very few reports on myocardial bridging in children, and it is usually seen in the setting of hypertrophic cardiomyopathy/left ventricular hypertrophy. Whether it is an independent risk factor for sudden death has been controversial. Most cases are clinically silent and only rare cases are symptomatic with chest pain, myocardial ischemia, infarction, and even sudden death, especially during severe exercise [34, 35]. Cardiac MR can identify the coronary artery anatomy as well as infarct. Aortic stenosis Aortic valvular stenosis in children is caused by dysplastic aortic valve, usually bicuspid or less commonly unicuspid. Cardiac MR can identify the morphology of leaflets. Cine MRI sequences show restricted systolic opening of the aortic valve leaflets along with systolic flow acceleration. The valve area can be measured and the velocity and peak gradient of the stenotic jet can be quantified using velocity-encoded phasecontrast MRI. Severe aortic stenosis can result in myocardial ischemia and fibrosis because of an imbalance between myocardial oxygen demand and supply. This fibrosis manifests as late gadolinium enhancement in a diffuse subendocardial pattern [36, 37] (Fig. 6). It has been shown that subendocardial LGE in adolescents who underwent successful balloon valvuloplasty in infancy corresponds to fibroelastosis on pathology and is associated with diastolic dysfunction [38]. The presence of diffuse LGE distinguishes aortic stenosis from a Fig. 5 Coronary fistula. a Coronal steady-state free precession (SSFP) cardiac MR image in a 16-year-old girl shows a large fistula (arrows) originating from the left coronary artery (*), which drained into the coronary sinus (not shown). There is also a small pericardial effusion. b Volume-rendered CT image shows the coronary fistula in detail (arrow), originating from left coronary artery (*) and draining into the coronary sinus (arrowhead). c Short-axis SSFP LGE cardiac MR image in the same girl shows near-full-thickness transmural infarct of the basal anteroseptum (arrow), secondary to myocardial steal phenomenon. LGE late gadolinium enhancement, LV left ventricle

8 Pediatr Radiol (2016) 46: Fig. 6 Aortic stenosis. Short-axis SSFP LGE cardiac MR image in a 6- year-old boy shows extensive late gadolinium enhancement involving the subendocardial and mid-myocardial regions (arrows), with sparing of the subepicardial region, caused by severe aortic stenosis and supply demand mismatch in hypertrophied myocardium that corresponds to endocardial fibroelastosis on histology. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession typical infarct, while the presence of aortic valvular abnormalities, normal signal from blood pool and normal T1 kinetics distinguishes it from cardiac amyloidosis. Non-ischemic cardiomyopathies Dilated cardiomyopathy Dilated cardiomyopathy is the most common type of cardiomyopathy in children [39]. Most of these cases (69%) are idiopathic, but other etiologies include myocarditis and inborn errors of metabolism [39]. Dilated cardiomyopathy is a heterogeneous disease in children. It frequently results in severe congestive heart failure requiring pharmacological treatment and even cardiac transplant, but some children remain stable or even show reverse remodeling with normalization of left ventricular function. Cardiac MR demonstrates left ventricular dilatation and global hypokinesis. In adults, linear mid-myocardial late gadolinium enhancement in a non-vascular distribution, usually in the ventricular septum, is seen in up to 28% of patients with idiopathic dilated cardiomyopathy from focal segmental fibrosis [40] (Fig.7). In 59% of these patients, no LGE is seen, which is likely because of diffuse fibrosis detection that is beyond the resolution of MRI. In 13% of people with idiopathic dilated cardiomyopathy, a subendocardial pattern of enhancement from infarct is seen in spite of normal coronary arteries in catheterization, a result of recanalization after an occlusive coronary event or embolization from minimal stenotic unstable plaque[40]. The presence of LGE, regardless of Fig. 7 Idiopathic dilated cardiomyopathy. Short-axis SSFP LGE cardiac MR image in a 9-year-old boy shows a linear mid-myocardial (arrow) pattern of enhancement, with sparing of the subendocardial and subepicardial region in the ventricular septum, suggestive of idiopathic dilated non-ischemic cardiomyopathy. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession its extent or distribution, is associated with adverse prognosis such as sudden cardiac death [41] because scar is a substrate for arrhythmia [42]. In children, a study performed on a group with dilated cardiomyopathy showed the presence of LGE in only 16% [43]. Eighty percent of these children had histopathological findings of lymphocytic myocarditis, with several patterns of LGE such as mid-wall, focal patchy types, right ventricle insertion site and transmural. The remaining 20% of children with LGE did not show any underlying cause on histopathology (i.e. idiopathic dilated cardiomyopathy) and demonstrated the classic mid-myocardial LGE as seen in adults. Based on this study, histologically proven myocardial fibrosis is rarely seen in late gadolinium enhancement MRI and it is not clear whether there is a different repair mechanism for fibrosis in children that enables favorable reverse remodeling [43]. The presence of LGE is useful for determining which children might benefit from cardioverter defibrillator (ICD) implantation. Hypertrophic cardiomyopathy Hypertrophic cardiomyopathy (HCM) is the second most common type of cardiomyopathy in children and is identified by otherwise unexplained left ventricular hypertrophy associated with non-dilated cardiac chambers. It is an autosomaldominant inherited abnormality of the cardiac muscle and many gene mutations predominantly involving sarcomere genes (majority in β- myosin, or cardiac myosin binding protein C gene) have been identified that cause left ventricular hypertrophy. Sarcomere mutations are found in approximately 65% of children and adults with familial HCM and in 40% of people with unexplained left ventricular hypertrophy [44].

9 1104 Pediatr Radiol (2016) 46: HCM can be asymptomatic or present with chest pain, dyspnea, syncope, palpitations or sudden death. HCM has variable phenotypical expression. The most common pattern of HCM is an asymmetrical hypertrophy of the basal ventricular septum; variants include asymmetrical hypertrophy of the mid or apical segments (Yamaguchi type) and mass-like, concentric and spiral types. Cardiac MR is useful in the evaluation of morphology and the quantification of left ventricular outflow obstruction, systolic anterior motion of mitral valve and mitral regurgitation, and it is the ideal modality to delineate papillary muscle abnormalities. LGE is seen in 40 80% of adults with HCM [45] because of increased myocardial collagen, likely a result of replacement fibrosis from microvascular ischemia caused by small coronary arteriole dysplasia [46]. Other proposed causes include myofibrillar disarray or mutation-induced deposition of connective tissue. LGE is seen in a patchy, fine pattern, typically in the hypertrophied portions of myocardium (Fig. 8), often at right ventricular insertion points. LGE can also be seen in non-hypertrophied segments. Recent studies in children have shown LGE in 28 73% of children with HCM in a similar pattern as in adults mid-myocardial associated with myocardial hypertrophy [47 49]. LGE has clinical importance for determining the prognosis and management guidance. It is correlated with adverse clinical outcomes including lower ejection fraction [50], arrhythmia [45] and sudden cardiac death in both children and adults with HCM [48, 49, 51]. In children it has been shown that increased left ventricular mass is associated with non-sustained ventricular tachycardia and worsened diastolic function. There is a significant relationship between the extent of LGE and the presence of nonsustained ventricular tachycardia [52]. LGE is also associated with worsened diastolic function [52]. Extensive LGE might indicate the need for ICD placement, although there is no conclusive evidence [45]. Arrhythmogenic right ventricular dysplasia/cardiomyopathy ARVD/C is a rare inherited cardiomyopathy characterized by structural and functional abnormalities of the right ventricle caused by replacement of myocardium with fibro-fatty tissue leading to arrhythmias and progressive right ventricular dysfunction. ARVD/C is a well-recognized cause of sudden cardiac death in young athletes. Autosomal-dominant inheritance and variable penetration caused by mutations in desmosomal protein genes has been described. The diagnosis of ARVD/C is based on recently modified taskforce criteria that include global or regional dysfunction and structural alterations, family history, tissue characterization of wall, arrhythmias, and repolarization and depolarization abnormalities [53]. On cardiac MR the major criterion to diagnose ARVD/C is regional Fig. 8 Hypertrophic cardiomyopathy. a Short-axis SSFP LGE cardiac MR image in a 17-year-old boy shows severe asymmetrical hypertrophy of the ventricular septum. There is fine, patchy mid-myocardial LGE within hypertrophied segments (arrows) as well as non-hypertrophied areas (arrowhead), consistent with interstitial fibrosis in a pattern specific for hypertrophic cardiomyopathy. b Four-chamber SSFP LGE cardiac MR image in a 16-year-old girl shows asymmetrical hypertrophy of the apical ventricular myocardium with extensive patchy LGE of the apical segment (arrows), consistent with apical variant hypertrophic cardiomyopathy. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession right ventricular akinesis/dyskinesis/dyssynchrony along with elevated right ventricular end-diastolic volume (>110 ml/m 2 in boys, >100 ml/m 2 in girls) or decreased right ventricular ejection fraction ( 40%) [53]. Fat infiltration in a thinned right ventricle wall might be seen in 75% of cases (mostly adults), usually at the right ventricle inflow, outflow and lateral wall [54, 55]. Although LGE is not part of the proposed diagnostic criteria, it has diagnostic and prognostic value [56, 57]. Tandri et al. [56] identified right ventricular LGE caused by fibrofatty deposition in 88% of adults and older adolescents with ARVD/C (Fig. 9). LGE was seen in the triangle of dysplasia, which was described as the sub-tricuspid portion, outflow tract, apex and mid-free wall [54]. More recent studies have

10 Pediatr Radiol (2016) 46: Fig. 9 Arrhythmogenic right ventricular dysplasia/cardiomyopathy. Right ventricular horizontal long-axis SSFP LGE cardiac MR image in a 16-year-old girl shows dilated right ventricle with thinning of the wall. There is diffuse enhancement of the right ventricle myocardium (arrows), indicative of fibrous replacement of right ventricle wall in this girl with ARVD. LGE late gadolinium enhancement, LV left ventricle, RV right ventricle, SSFP steady-state free precession excluded the apex from the triangle of dysplasia and have also shown LGE in the left ventricle in 61% of cases [55]. On the other hand, a study focusing on children and younger adolescents found LGE in 13% (3 out of 23) of children with definite ARVD/C per revised taskforce criteria, suggesting that it has limited value in diagnosis in early stages of disease in children and adolescents [58]. However, when present, LGE had excellent correlation with fibro-fatty changes on endomyocardial biopsy and was associated with inducible arrhythmia on electrophysiology [56]. Treatment includes antiarrhythmic agents, intracardiac defibrillator (ICD) placement and radiofrequency ablation. Left ventricular non-compaction Left ventricular non-compaction is a rare condition characterized by the presence of non-compacted left ventricular myocardium caused by abnormal persistence of primitive embryonal cardiac sinusoids, which typically regress and become compacted in a normal fetus. Multiple mutations have been described including taffazin, β-myosin-heavy chain, α- cardiac actin and cardiac troponin T. Left ventricular noncompaction is most commonly diagnosed in the first year after birth and can present with ventricular arrhythmias, ventricular dysfunction and thromboembolism, although some children are asymptomatic until adolescence. On cardiac MR a diagnosis is made by the presence of exaggerated ventricular trabeculations, with a ratio of non-compacted to compacted myocardium >2.3 in diastole [59]. LGE has been reported in 25 40% of the patients meeting the cardiac MR criteria for left ventricular non-compaction [60, 61] (Fig. 10), probably a Fig. 10 Left ventricular non-compaction. Four-chamber SSFP LGE cardiac MR image in a 7-year-old girl shows dilated left ventricle with prominence of trabeculations in the mid and apical ventricular segments (ratio of compacted to non-compacted myocardium -3.1), with fine subtle enhancement of the trabeculations (arrows) consistent with left ventricular non-compaction. The LGE was distinguished from slow flow by correlating with cine SSFP images at the same level (not shown). LGE late gadolinium enhancement, SSFP steady-state free precession result of coronary microcirculatory dysfunction or embolism. The distribution of LGE was heterogeneous, with 6% showing subendocardial, 68% mid-myocardial, 11% subepicardial and 15% transmural patterns of enhancement [61]. There is an inverse correlation between the presence or extent of LGE, and left ventricular ejection fraction in these patients [62]. Presence of LGE is associated with arrhythmia [62]. Management includes heart failure treatment, ICD placement and anticoagulation. Sarcoidosis Cardiac sarcoidosis is characterized by presence of nonspecific inflammatory changes/non-caseating granulomas in the myocardium. Cardiac involvement is seen in 5% of patients with multisystemic sarcoidosis and is uncommon in children [63]. Clinical presentations include cardiac failure, arrhythmia, acute chest pain and pericardial effusion. On cardiac MR in the acute phase of the disease, there may be myocardial thickening and edema, along with wall motion abnormalities. In the chronic phase of the disease there is no myocardial thickening or edema, but wall motion abnormalities are sometimes seen. LGE is seen in about 25% of patients with systematic sarcoidosis caused by granulomatous infiltration or fibrosis. LGE has nodular morphology and is seen in a subepicardial or midmyocardial pattern and can be seen in both acute and chronic phases (Fig. 11). Enhancement is more common in the basal septum, more intense on the right ventricular side of the septum. A transmural pattern of enhancement might be seen in

11 1106 Pediatr Radiol (2016) 46: Fig. 11 Sarcoidosis. Short-axis SSFP LGE cardiac MR image in a 16- year-old girl with cardiac sarcoidosis shows subepicardial pattern of enhancement (arrows). LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession chronic burnt-out cases [63]. The extent of LGE is directly correlated with duration of disease and left ventricular volume and inversely correlated with ejection fraction [64]. LGE is an important prognostic factor and its presence regardless of left ventricular enlargement or impaired ejection fraction increases the risk of death or potentially lethal events, including aborted sudden cardiac death or appropriate ICD discharge and other adverse events such as ventricular tachycardia, by more than 30 times [65]. Treatment includes steroids, and cardiac MR can be used to assess response to therapy. Although there are no established guidelines for evaluation of treatment response using cardiac MR, a few studies have shown favorable results. For instance, in a prospective study of 12 patients, all of the 6 receiving steroid therapy showed cleared or improved cardiac MR and LGE at 12-month follow-up, while the rest had worsened or remained stable. The stability, improvement or worsening of follow-up cardiac MR was correlated with clinical stability, improvement or worsening, respectively [66]. 69]. Distinguishing Fabry disease from HCM is important because the former is managed by enzyme replacement/ enhancement therapy and the latter by pharmacological therapy/surgery/icd. Decreased enzymatic activity in the blood can be diagnostic of Fabry disease, but in female carriers and some male patients with specific gene mutations cardiac involvement is the only manifestation with normal enzymatic activity [67]. Cardiac MR typically demonstrates concentric left ventricular thickening that is indistinguishable from symmetrical HCM. Late gadolinium enhancement imaging can help differentiate Fabry disease from HCM. In Fabry disease LGE is seen because of collagen deposition or myocarditis caused by cardiac infiltration [70]. Mid-myocardial or subepicardial pattern of LGE in the basal inferolateral wall is a characteristic feature of Fabry diseases [71] (Fig. 12). Although this segment can be involved in children with HCM, too, enhancement is seen in other segments in HCM and might also involve the subendocardial region [71]. Extensive enhancement might be associated with regional wall motion abnormalities and wall thinning. Presence of LGE has been associated with adverse prognosis, including arrhythmia and sudden cardiac death [72]. MRI is also useful in monitoring response to enzyme replacement therapy, which shows decreased left ventricular mass. Danon disease Danon disease is a rare lysosomal storage disease caused by mutation of lysosomal-associated membrane protein-2 (LAMP2) gene with X-linked dominant inheritance. Accumulation of intracytoplasmic autophagic vacuoles results in severe cardiac hypertrophy, heart failure, variable mental Storage disorders Anderson Fabry disease Anderson Fabry disease is an X-linked storage disorder caused by deficiency of α-galactosidase A and resulting in intracellular accumulation of glycosphingolipid in different tissues. Cardiac involvement presents with concentric left ventricular thickening, heart failure and arrhythmias, which are fairly nonspecific and sometimes mimic HCM. Fabry disease accounts for 3% of patients with left ventricular hypertrophy [67]. More important, it has been diagnosed in 6 12% of people with suspected late-onset symmetrical HCM [68, Fig. 12 Anderson Fabry disease. Short-axis SSFP LGE cardiac MR image in an 11-year-old girl with Anderson Fabry disease shows a focal area of mid-myocardial enhancement in the basal inferolateral wall (arrow). LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession

12 Pediatr Radiol (2016) 46: retardation, skeletal myopathy, ophthalmic abnormalities, elevated creatine kinase, liver enzymes and Wolff Parkinson White syndrome in young boys. Female carriers present late with milder symptoms. Diagnosis is confirmed by skeletal muscle or endomyocardial biopsy. Cardiac phenotype is characterized by early onset and poor prognosis. Four percent of patients diagnosed as HCM have Danon disease [73]. Cardiac MR shows concentric left ventricular thickening. Myocardial edema and perfusion defects have also been described. LGE shows a subendocardial, transmural [74] or mid-myocardial pattern in a non-vascular distribution [75] (Fig.13). LGE has been described in anterior lateral and inferior walls, with sparing of the ventricular septum between the right ventricular insertion points reported in some series [76]. Septal enhancement is occasionally seen. The presence of this pattern of LGE with hypertrophy narrows the differential diagnosis. Danon disease should be suspected in a child with concentric hypertrophy and with LGE relatively sparing the septum. Muscular dystrophies Muscular dystrophies are X-linked neuromuscular disorders caused by abnormal dystrophin, which results in necrosis of cardiac and skeletal muscle fibers and their replacement with connective tissues and fat. Duchenne dystrophy is caused by absence of dystrophin and Becker dystrophy is caused by decreased/abnormal dystrophin. As a result of advances in respiratory care, cardiac abnormality is the most common cause of death in these children. Cardiac abnormalities include dilated cardiomyopathy, arrhythmia and sudden death. LGE has been reported in 32 89% of people with Duchenne dystrophy as a result of interstitial fibrosis and fat replacement [77]. LGE is more common in the free wall segments (43%) in a subepicardial or mid-myocardial pattern [77 80] compared to septal segments (5%), with septal LGE only seen in conjunction with free wall enhancement and more frequently in older patients [78]. In the free wall, anterolateral and inferolateral segments are the most commonly involved segments [78, 79] (Fig. 14). LGE is progressive, may become transmural in severe cases [79] and increases with age [78]. Current studies have shown that LGE cardiac MR is an important clinical tool in both diagnosis and management of muscular dystrophies. Duchenne dystrophy should remain in the differential list for a dilated cardiomyopathy with subepicardial LGE. Additionally, it has been shown that LGE on cardiac MR can indicate cardiac involvement well before the presence of cardiac symptoms [81] or electrocardiographic (ECG) or echocardiographic abnormalities [80], even in female carriers [82]. Moreover, the extent of LGE is related to lower left ventricular ejection fraction and death [78, 79]. LGE cardiac MR can also guide the timing for pacemaker/icd placement based on the extent of right heart involvement. Inflammatory disorders Myocarditis Myocarditis is usually caused by an acute viral infection, which can be enterovirus, adenovirus, parvovirus B19, or human herpesvirus-6. Clinically there is acute chest pain, elevation of cardiac enzymes and ECG abnormalities such as ST segment elevation. Cardiac MR can show regional wall motion Fig. 13 Danon disease. Short-axis SSFP LGE cardiac MR image in a 9- year-old girl with Danon disease shows severe concentric thickening with patchy mid-myocardial enhancement (arrows) and relative sparing of the septum. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession Fig. 14 Duchenne dystrophy. Four-chamber SSFP LGE cardiac MR image in a 14-year-old girl with Duchenne dystrophy shows dilated left ventricle with near full thickness, patchy enhancement in the basal and mid-lateral segments (arrows). LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession

13 1108 Pediatr Radiol (2016) 46: abnormalities and also edema in the affected myocardium on T2-weighted images, which is more common in the basal inferolateral wall. Early gadolinium enhancement is seen because of hyperemia and capillary leak [83]. LGE may be seen in the acute phase of myocarditis because of cellular damage and expansion of extracellular space, in a mid-myocardial or subepicardial distribution (Fig. 15), most commonly in the posterior and lateral walls [84]. With replacement of necrosis by fibrotic tissue, irreversible injury results and this also produces LGE in a similar distribution as above [83]. Edema and early LGE resolve with resolution of acute myocarditis, whereas persistent LGE indicates irreversible injury [85]. Persistence of LGE beyond 4 weeks might indicate a complicated course with development of fibrosis, because viral clearance occurs in few days after infection and myocardial inflammation usually clears by 2 3 weeks [83, 86]. There may be variable distribution of enhancement based on the virus type. For example, the parvovirus B19 myocarditis has been shown to affect the basal inferolateral segment in a mid-myocardial/subepicardial distribution (Fig. 15) and is generally associated with good recovery, while human herpesvirus-6 myocarditis has been shown to affect the ventricular septum, in a linear mid-myocardial pattern, and is generally associated with rapid progression of heart failure [87](Fig. 15). Presence of LGE is associated with poor outcomes [84]. Pericarditis Pericarditis in children is often of infectious etiology, usually associated with myocarditis. Other etiologies include connective-tissue disorders, myocardial infarction, radiation, uremia and idiopathic. Acute pericarditis presents with chest pain, pericardial rub, fever and ST segment elevation. Constrictive pericarditis presents with dyspnea, fatigue, edema, ascites and weakness. Cardiac MR is increasingly used in the diagnosis and management of pericarditis. Acute pericarditis manifests with pericardial thickening (>4 mm) and pericardial effusion. LGE sequence shows intense focal or diffuse pericardial enhancement (Fig. 16). Studies have shown the correlation between pericardial enhancement and inflammation [88, 89]. Pericardial constriction is a sequela of chronic pericarditis from non-compliant and thickened pericardium. Cardiac MR shows the functional abnormalities such as diastolic septal bounce, abrupt diastolic cessation and exaggerated ventricular interdependence, which manifests as increased diastolic septal flattening with inspiration. Although pericardial constriction is usually managed with surgery, recent studies have shown that transient constriction can be seen from pericardial inflammation or effusion [90]. Hence, in constrictive patients where cardiac MR shows LGE as evidence of pericardial inflammation, the constriction might be reversible with aggressive anti-inflammatory therapy, thus obviating the need for surgery [90]. Masses Cardiac MR has a unique advantage in the evaluation of cardiac masses because of its tissue characterization capabilities, which enable narrowing of differential diagnoses. Cardiac mass evaluation includes T1-weighted, T2-W, fat-saturated and diffusion sequences along with early and delayed contrast-enhanced sequences. Fig. 15 Myocarditis. a Short-axis SSFP LGE cardiac MR image in an 11-year-old boy who presented with acute-onset chest pain, elevated enzymes and ST segment elevation shows an area of sub-epicardial to mid-myocardial enhancement in the lateral wall (arrow). This boy had parvovirus B19 myocarditis. b Short-axis SSFP LGE image in a 9-yearold boy with acute-onset chest pain and elevated enzymes shows linear mid-myocardial enhancement in the mid-ventricular septum (straight arrows) and also subepicardial enhancement (curved arrow) inthe lateral wall, consistent with acute myocarditis. This boy had human herpesvirus-6 myocarditis and progressed to heart failure. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession

14 Pediatr Radiol (2016) 46: longer inversion time (>500 milliseconds) is also valuable in differentiating thrombus from neoplasm, because a thrombus remains dark at this inversion time (Fig. 17), whereas a neoplasm often has higher signal at these inversion times [91]. Neoplasms Primary cardiac tumors are rare. Ninety percent of primary pediatric cardiac tumors are benign and 10% are malignant [92]. Benign neoplasms Fig. 16 Pericarditis. Three-chamber SSFP LGE cardiac MR image in an 18-year-old man with acute-onset chest pain and ST segment elevation shows diffuse circumferential enhancement of the thickened pericardium (arrows), consistent with acute pericarditis. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession Thrombus Thrombus is the most common cardiac mass in children. Higher predilection of thrombus is seen in those with central venous catheters and pro-thrombotic conditions and adjacent to dysfunctional myocardium. On cardiac MR, thrombus has intermediate to low signal on SSFP, T1-W and T2-W images. Often, distinguishing a thrombus from a cardiac neoplasm is challenging, and LGE sequence is very useful in making this determination. A thrombus has low signal intensity in LGE images and does not show enhancement (Fig. 17) unless it is vascularized in chronic stages. An LGE image obtained at a Rhabdomyoma, a hamartoma of myocardium, is the most common benign pediatric cardiac neoplasm (60% of childhood cardiac neoplasms) [92]. It is associated with tuberous sclerosis in one-third to one-half of cases. It is typically intramyocardial but can extend into the cardiac cavity. On cardiac MR, the signal characteristics are similar to those of a myocardium [93]. Although there might be early enhancement, no enhancement is seen on delayed images [94]. Fibroma is the second most common primary tumor in children. Most fibromas are found in infants during the first year of life. On cardiac MR it is isointense or slightly hyperintense in T1-W images and hypointense in T2-W images [95]. Fibroma typically does not have any enhancement in the early phase but often shows heterogeneous late gadolinium enhancement (Fig. 18) [96]. Low signal can be seen in the center of the neoplasm, either from calcification or poorly vascularized fibrous tissue [94]. Myxoma is less common in children, although it is the most common benign neoplasm in adults. On cardiac MR it is hypointense on T1-W images and hyperintense on T2-W Fig. 17 Thrombus. a Short-axis SSFP LGE cardiac MR image in a 16- year-old girl obtained at an inversion time of 290 msec (based on a T1 scout) shows a mass in the right atrium (RA) with no LGE (arrow). b Four-chamber SSFP LGE image in the same girl obtained with longer inversion time (600 msec) shows that the mass (arrow) remains low in signal even at longer inversion times (compared to myocardium, which has become grayish), which is consistent with the appearance of thrombus. LA left atrium, LGE late gadolinium enhancement, SSFP steady-state free precession

15 1110 Pediatr Radiol (2016) 46: Fig. 18 Fibroma. a Short-axis SSFP cardiac MR image obtained 1 min after contrast administration in a 12-year-old boy shows a mass adherent to the inferolateral wall of the left ventricle (straight arrow), demonstrating no early contrast enhancement. There is also a small pericardial effusion (curved arrow). b Short-axis SSFP LGE cardiac MR image in the same patient shows intense LGE of the mass (arrow), consistent with a fibroma. LGE late gadolinium enhancement, LV left ventricle, SSFP steady-state free precession images because of its high water content. LGE is typically heterogeneous [93]. Teratoma, lipoma and hemangioma are less common benign pediatric cardiac neoplasms. Malignant neoplasms Metastasis is the most common cardiac malignancy in children, times more common than primary neoplasms [92]. Secondary involvement is seen in leukemia, lymphoma, Wilms tumor, hepatoblastoma, neuroblastoma, Ewing sarcoma and osteosarcoma [96, 97]. There is a wide spectrum of presentation of metastases. This includes myocardial nodules (Fig. 19), pericardial nodules, pericardial effusion or diffuse myocardial infiltration. On cardiac MR, myocardial or pericardial nodules show low signal on T1-W and high signal on T2-W images. Malignant pericardial effusion is often associated with pericardial thickening and nodules, with loculated and hemorrhagic or serosanguineous effusion with high signal on T1-W images [98]. Metastatic myocardial or pericardial nodules have variable LGE (Fig. 20) [93]. Sarcoma is the most common primary cardiac pediatric malignancy, accounting for 95% of these cases [92]. The prognosis is poor because sarcoma is aggressive and infiltrative. It presents as a large mass, with extension to the pericardium in the form of nodules, effusion or hemorrhage. It shows intermediate signal in T1-W images, high signal on T2-W images and heterogeneous LGE [95]. Fig. 19 Metastatic sarcoma. Four-chamber SSFP LGE cardiac MR image in a 16-year-old boy with soft-tissue sarcoma of the right lower extremity shows multiple focal masses in the myocardium and pericardium with heterogeneous LGE (arrows), consistent with metastatic disease. LGE late gadolinium enhancement, LV left ventricle, RV right ventricle, SSFP steady-state free precession Fig. 20 Leukemia. Four-chamber SSFP LGE cardiac MR image in a 17- year-old boy shows diffuse heterogeneous enhancement of the myocardium (straight arrows), consistent with leukemic infiltration in this boy. Some focal masses do not show LGE (arrowheads). Note the small pericardial effusion with very low signal (curved arrows). LGE late gadolinium enhancement, LV left ventricle, RV right ventricle, SSFP steady-state free precession