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Published in final edited form as: Int J Cardiovasc Imaging. 2013 Aug 15;29(8):1787–98. doi: 10.1007/s10554-013-0276-9

The emerging role of cardiovascular magnetic resonance in the evaluation of Kawasaki disease

Sophie Mavrogeni ✉, George Papadopoulos 1, Tarique Hussain 2,3, Amedeo Chiribiri 4, Rene Botnar 5, Gerald F Greil 6,7
PMCID: PMC7611141  EMSID: EMS128773  PMID: 23949280

Abstract

Kawasaki disease (KD) is a vasculitis affecting the coronary and systemic arteries. Myocardial inflammation is also a common finding in KD post-mortem evaluation during the acute phase of the disease. Coronary artery aneurysms (CAAs) develop in 15–25 % of untreated children. Although 50–70 % of CAAs resolve spontaneously 1–2 years after the onset of KD, the remaining unresolved CAAs can develop stenotic lesions at either their proximal or distal end and can develop thrombus formation leading to ischemia and/or infarction. Cardiovascular magnetic resonance (CMR) has the ability to perform non-invasive and radiation-free evaluation of the coronary artery lumen. Recently tissue characterization of the coronary vessel wall was provided by CMR. It can also image myocardial inflammation, ischemia and fibrosis. Therefore CMR offers important clinical information during the acute and chronic phase of KD. In the acute phase, it can identify myocardial inflammation, microvascular disease, myocardial infarction, deterioration of left ventricular function, changes of the coronary artery lumen and changes of the coronary artery vessel wall. During the chronic phase, CMR imaging might be of value for risk stratification and to guide treatment.

Keywords: Cardiovascular magnetic resonance, Kawasaki disease, Myocarditis, Myocardial perfusion, Coronary aneurysm, Myocardial infarction

Current understanding

Kawasaki disease (KD) is a specific type of systemic vasculitis that affects mainly medium-sized arteries, with a particular predilection for the coronary arteries. Currently, it has replaced the acute rheumatic fever as the most common cause of acquired heart disease in children in the USA [1]. The incidence of coronary artery aneurysms in patients with KD was 25 %, but dropped to 5–10 % after the application of immunoglobulin treatment [2]. Aneurysms may also occur in celiac, mesenteric, femoral, renal and other body arteries [3]. There are some data in the literature about the incidence of myocarditis during the acute phase of KD and all of these refer to cases with severe LV dysfunction [4–6]. However, myocarditis is a standard finding in post-mortem and biopsy studies [1]. In contrary to viral myocarditis, which is considered to be the result of injury by virus infiltration and resulting host immune response, the myocarditis in KD is characterized by inflammatory infiltration from the coronary arteries to the interstitial myocardium. Therefore myocardial necrosis is rarely observed [5]. Pericarditis and valvulitis may also be found during the course of myocardial inflammation [4].

During the acute phase, the endothelial and smooth-muscle cells are affected by the inflammatory infiltration of the vessel wall and, as a consequence, the vessel loses its structural integrity, resulting in dilatation of artery or aneurysm formation (Figs. 1, 2). Fibrosis of the vessel wall leads to stenotic lesions on either end of the aneurysm. Consequently, low blood flow within the aneurysm pre-disposes to thrombus formation leading to ischemia and/or infarction.

Fig. 1. Coronary magnetic resonance angiography vs X-ray coronary angiography in Kawasaki Disease.

Fig. 1

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Left anterior descending coronary artery (LAD) with a fusiform aneurysm. Coronary MRA (left), X-ray angiography (right) [17]

Fig. 2. Coronary MRA vs X-ray coronary angiography in Kawasaki disease.

Fig. 2

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Aneurysmatic RCA from a patient with Kawasaki disease. MRA (left), X-ray angiography (right). Mavrogeni S Onassis Cardiac Surgery Center, Athens, Greece

Risk factors for developing aneurysms include male gender, age younger than 1 year or older than 5 years, persistent fever refractory to treatment, anemia, hypoal-buminemia and a high C-reactive protein levels at presentation [7].

Almost half of the children with coronary aneurysms (CAAs) during the acute phase of the disease have angiographic normal vessels 1–2 years later [8]. Usually 50–70 % of CAAs resolve spontaneously 1–2 years after the onset of KD. Smaller aneurysms are more likely to regress than larger ones [2]. Other variables associated with greater likelihood of regression include age younger than 1 year at onset of KD, fusiform versus saccular morphology and location of the CAA in the distal part of coronary artery [2]. Unresolved CAAs persist and stenotic lesions and/or thrombus develop. Rarely a CAA may rupture within the first few months after onset of the disease. Myocardial infarction due to either thrombosis of an aneurysm or due to a stenotic lesion is the main cause of death in KD. The risk of infarction is highest during the first year after the onset of the disease. Under these circumstances, the serial evaluation of size and location of CAAs is necessary for risk stratification and treatment decisions. KD is a challenge for the clinician, as the development of aneurysms is usually clinically silent and may be recognized many years after the diagnosis, due to late complications such as myocardial infarction and subsequent sudden death [9, 10]. Furthermore, apart from the coronary anatomy, the myocardial perfusion pattern during rest and stress may be of great value for defining the presence or absence of microvascular myocardial disease.

In 2004, the American Heart Association (AHA) published guidelines for follow-up of patients with KD based on a consensus of experts [2]. Patients are stratified into five risk levels according to their relative risk of myocardial ischemia and infarction (Table 1). Serial echocardiography is recommended for patients without CAAs or with transient coronary artery dilatations normalizing within the first 6–8 weeks after the acute presentation of the disease (risk levels I–II). For patients with persistent CAAs, serial nuclear stress tests and conventional coronary angiography are recommended in addition to regular echocardiography (risk levels III–V).

Table 1. Summary of the 5 risk levels in Kawasaki disease according to AHA guidelines.

Risk Level I Patients with no coronary artery changes on Echo at any stage of the illness
Risk Level II Patients with transient coronary artery ectasia or dilatation (disappearing within the initial 6–8 weeks after the onset of illness
Risk Level III Patients with isolated (solitary) small to medium (>3-mm but >6-mm, or z score between 3 and 7) coronary artery aneurysm in >1 coronary arteries on echocardiography or angiography
Risk Level IV Patients with >1 large coronary artery aneurysm (>6 mm), including giant aneurysms, and patients in whom a coronary artery contains multiple (segmented) or complex aneurysms without obstruction
Risk Level V Patients with coronary artery obstruction confirmed by angiography
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However, the imaging modalities recommended in the AHA 2004 guidelines have some significant limitations [2]. Echocardiography is the first choice for routine coronary artery surveillance and is used to screen patients with KD for the presence of coronary artery pathology [2, 11]. However, with echocardiography it is only usually the proximal part of the coronary arteries that can be visualized adequately. CAA stenosis can be missed as can distal coronary artery aneurysms. In addition, echocardiography may be limited by operator dependency and becomes progressively more difficult when children grow and body size increases [12]. Nuclear perfusion scans are recommended to address ventricular function in relation to vascularization and ischemia with modest specificity, while resulting in high radiation exposure [13–15]. Conventional coronary angiography is the gold standard for coronary artery lumen evaluation and is able to detect CAAs, coronary artery stenosis and coronary occlusion. However there are risks associated with its invasive nature and with the exposure to contrast agents and radiation [16].

Cardiac Magnetic Resonance (CMR) has emerged as a non-invasive and radiation-free imaging modality for evaluation of coronary arteries in both childhood KD and adult ischaemic heart disease by delineating the proximal and mid-portion of the coronary artery lumen and vessel wall [17–20], cardiac function and myocardial perfusion. CMR can also be used for pharmacological stress testing to assess ischemia. In combination with delayed contrast enhancement viable and non-viable myocardium can be differentiated, as show in the context of adult ischaemic heart disease [21–24].

An algorithm for imaging patients with KD using different imaging techniques has been suggested [25]. However, given the recent rapid development of CMR, a rediscussion of the various imaging protocols of KD during the acute and chronic phase is warranted.

CMR in KD: when and how?

Acute phase

During the acute phase a complete evaluation of the coronary artery lumen and vessel wall, ventricular function, myocardial inflammation and myocardial fibrosis (either due to inflammatory process or due to myocardial infarction) would be desirable for KD patients with risk levels III–V and/or left ventricular wall motion abnormalities or dilatation. However, until now its utility in younger patients has not been well demonstrated and CMR did not prove a clear superiority over echocardiography during this acute phase, particularly in KD with less severe coronary abnormalities.

Coronary artery imaging by CMR

The presence of CAA needs serial evaluation for risk stratification. Although transthoracic echocardiography is usually sufficient in young children for the proximal portion of the coronary arteries, adequate visualization of the distal coronary arteries becomes progressively more difficult, particularly as children grow. According to previous publications, CMR of the coronary artery lumen using navigator techniques to suppress respiratory motion has excellent correlation with X-ray coronary angiography and can be used as a reliable alternative to X-ray coronary angiography for definition of CAAs in KD patients [17, 18]. Recently, the application of free-breathing techniques in children with KD and congenital heart disease, using the whole-heart approach, successfully detected abnormalities of the coronary artery lumen, resulting in improved risk stratification and monitoring of therapy [26, 27] (Figs. 3, 4). Additionally, in a recently published study, it was shown that T2-STIR CMR enabled the detection of coronary artery wall oedema in animal models and this could, therefore, be used as a non-invasive diagnostic tool for the evaluation of inflammatory coronary artery vessel wall activity [28]. Coronary artery lumen imaging has been successfully performed in children younger than 1 year of age [29] (Fig. 5). However, further large multicentre studies are needed to establish the feasibility and limitations of quantitative assessment of the coronary artery lumen in comparison with echocardiography, CT coronary angiography and X-ray angiography in children. Current limitations of coronary MRA are: (1) its relatively low spatial resolution resulting in lower diagnostic accuracy for evaluating steno-occlusive coronary lesions in KD; (2) the long examination time and (3) the necessity for general anaesthesia or sedation in young children. However, CMR does allow both functional and wall motion evaluation of both ventricles and it is the current gold standard for ventricular function assessment [30].

Fig. 3.

Fig. 3

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Good agreement between the lateral X-ray angiogram (a) and the corresponding CMRA image (b) for detection of a right CAA in a 7.8-year-old boy (see also Fig. 5) with KD. MR images were acquired with a wholeheart 3D SSFP technique without the use of contrast agents. G. F. Greil, KCL London

Fig. 4.

Fig. 4

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Three year old patient with a giant aneurysm (*) in the left main and proximal left anterior descending. The left circumflex (arrow) comes of the distal end of the giant coronary aneurysm (*). The aneurysm is shown from anterior with a volume rendered whole heart three dimensional steady-state-free precession (3D SSFP) dataset (a) and after selective injection in the left coronary artery in the cardiac catheterization laboratory (b). G. F. Greil, KCL London

Fig. 5.

Fig. 5

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Images were acquired with a 2-D DIR black-blood segmented turbo spin-echo technique in a 7.8-year-old boy with Kawasaki disease. Sequential cross-sectional views of the aneurysm demonstrate a thickened vessel wall (arrows) at three different locations (a, b and c). G. F. Greil, KCL London

CT technology is rapidly evolving and its use is now discussed as an alternative to invasive coronary artery angiography. A recent study showed a superiority for coronary lumen assessment by CT in KD in comparison to coronary MRA.1

The main advantage of coronary CT is the high resolution isotropic acquisition of the heart and the coronary arteries with a voxel size of approximately 0.5 mm3 [31]. Additionally, coronary vessel wall thickness, calcification and areas of thrombosis may be assessed. High-pitch and wide detector array cardiac CT technology allows very rapid data acquisition, typically allowing complete imaging of cardiac structures within an acquisition period of less than 350 ms. This rapid acquisition greatly reduces the requirement for general anaesthesia or sedation. With the most recent CT technology, these studies may often be performed with a ‘feed and wrap” technique in a free breathing child [31]. However, major disadvantages still remain with coronary CT. The temporal resolution of cardiac CT is limited in currently in the order of 135–175 ms, although this may be reduced to 75 ms with dual source CT scanners [31]. Hence, rapid heart rates associated with most paediatric studies may lead to blurring of the coronary arteries and the assessment of coronary artery stenosis may be limited. Furthermore, the radiation dose associated with repeated examinations is problematic. Although very low dose acquisition <0.3 mSv) is currently possible [32], high or irregular heart rates frequently necessitate techniques such as increased phase acquisition, multi-segment reconstruction or retrospective gating and these techniques increase radiation exposure. Assessment of myocardial perfusion and ventricular function with CT increases the amount of radiation needed even further. Experience with this technology in the paediatric population is very limited.

Detection of myocardial inflammation by CMR

Myocardial inflammation is very common during the acute phase of CMR (~ 100 % of cases in post-mortem, biopsy and nuclear medicine studies) [2, 4]. According to recent pathology studies in KD, myocarditis develops earlier than epicardial coronary arteritis. Myocardial inflammation peaks 10 days after onset of the disease and then disappears gradually after 20 days. The distribution pattern of the myocarditis is irregular, including the entire heart, the epicardial layer or the base of the heart [33].

CMR can contribute to the diagnosis of myocardial inflammation using three types of images: T2-weighted (T2-W); early T1-weighted images acquired at 1–2 min after Gadolinium injection and delayed Gadolinium enhanced images acquired 15–20 min after the injection of contrast agent. T2-W imaging is a method which indicates the tissue free water content. This water content is increased in inflammation or necrosis, such as during myocardial infarction or myocarditis. However, it is not possible to differentiate between necrosis and inflammation only by the use of T2-W images. Early and delayed gadolinium enhancement images need to be obtained (Fig. 6). Early myocardial hyper-enhancement after gadolinium administration is due to increased membrane permeability or capillary blood flow. Conversely, the presence of contrast agent accumulation in the late Gadolinium enhanced images (15–20 min after contrast injection), is due to slower contrast agent wash out in fibrotic and necrotic tissue. A combined CMR approach using T2-W, early and late Gadolinium enhancement had a sensitivity of 76 %, a specificity of 95.5 % and a diagnostic accuracy of 85 % for the detection of myocardial inflammation from other causes [34, 35]. Myocarditis in KD has been identified by CMR during both the acute and the convalescence phase of the disease and also in KD in adults [6, 36–38]. In a recent longterm follow-up CMR study evaluating the cardiac function of patients with KD, no difference in cardiac function between KD patients and controls was observed, except in the a subgroup of patients with ischemic heart disease due to severe coronary artery pathology. However, multicenter follow-up data regarding myocarditis in KD are not available for final conclusions yet [39].

Fig. 6.

Fig. 6

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CMR reveals myocardial inflammation and coronary artery ectasia during the acute phase of Kawasaki disease. Coronary MRA indicative of LAD ectasia (left). T1-w image before and after Gd-DTPA injection (middle and right). The right image shows increased relative myocardial enhancement compared to the middle [36]

Myocardial function

Echocardiography is usually sufficient in most patients with KD with normal LV function, normal wall motion and no pericardial effusion. However, steady-state free precession (SSFP) cine imaging is a reliable technique to evaluate myocardial function and wall motion in specific cases with poor acoustic windows or unclear right ventricle (RV) function. The major advantage of CMRI compared to echocardiography is its excellent reproducibility. Therefore CMRI can detect minimal changes in ventricular volumes and ejection fraction during follow up [30, 40].

Myocardial fibrosis

CMR is the most reliable noninvasive imaging technique to detect and quantify scar or fibrotic tissue due to irreversible myocardial damage. Following acute ischemic injury, the myocardial distribution volume of gadolinium is increased, as a consequence of sarcolemmal rupture and abnormal washout kinetics. Imaging within the first few minutes after contrast agent administration is the method of choice to delineate microvascular obstruction (MVO), which prevents contrast delivery to the infarct core and thus results in low signal on T1-weighted imaging [41]. Both acute and old infarctions without MVO retain contrast agent and therefore appear bright [42–44]. The preferred imaging time for scar detection is between 10 and 20 min after contrast agent administration, when the contrast between scar, normal myocardium and blood pool is maximal. This method is referred to in the literature as late gadolinium enhancement and is the reference standard for the in vivo assessment of myocardial scar [44]. CMR can detect infarction in as little as 1 cm3 of tissue, substantially less than other in vivo methods such as echocardiography and nuclear techniques. CMR has shown excellent agreement with histology in animal and human studies [44]. It is also of value in the detection of RV infarction [45–47]. It is also important to note, that CMR can detect subendocardial myocardial infarction missed by SPECT or PET [48]. The extent of scar on CMR predicts the potential for functional recovery after revascularisation in adult ischaemic heart disease [42–44] (Figs. 7, 8).

Fig. 7.

Fig. 7

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Magnetic resonance coronary angiography and viability evaluation in chronic phase of Kawasaki disease. Coronary magnetic resonance angiography with RCA aneurysm (left). Contrast-enhanced CMR, indicative of sub-endocardial inferior infarction in the same patient (right) [30]

Fig. 8.

Fig. 8

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Coronary artery and viability evaluation during the convalescence of Kawasaki disease. Coronary MRA (left) showing an RCA aneurysm (arrow). Late gadolinium enhanced image (right) showing a transmural, inferior myocardial infarction (arrow) in the same patient [6]

Even though the use of immunoglobulin has reduced the incidence of coronary artery aneurysms, myocardial late gadolinium enhancement can be still detected by CMR in KD during the acute phase, due to either inflammation or myocardial infarction [6, 30, 39]. Furthermore, in adult ischaemic heart disease, not only the presence but also the amount of scar plays an important role in the patient’s prognosis, because there is evidence that even a small area of LGE (<2 % of LV mass) was associated with a greater than sevenfold increase in risk for a major adverse cardiac event [49].

Chronic phase

The development of CAA and coronary artery stenosis is of great importance during this phase. Particularly for older children, echocardiography may not be sufficient due to limited acoustic windows. In this case, coronary magnetic resonance angiography using a whole-heart approach can successfully detect CAAs [26, 50]. Additionally, wholeheart CMRA in adult ischaemic heart disease, is useful for predicting the future risk for cardiac events in patients with suspected coronary artery disease [49, 51]. Recently, evaluation of the coronary artery vessel wall has been successfully performed [52, 53], but data in KD are currently limited [26]. However, anatomic evaluation alone is not sufficient to successfully stratify risk in KD patients. Studies in patients with atherosclerotic coronary artery disease have shown that the relationship between the degree of stenosis and the influence on myocardial perfusion is complex. For example, marginal coronary stenosis can induce significant myocardial ischemia [54].

According to these data, the evaluation of KD with known significant coronary lesions during the acute phase, should include not only coronary artery anatomy but also rest and stress perfusion as well as viability assessment of the myocardium. Coronary artery lumenography is of special clinical value in order to identify the evolution of coronary lesions identified during the acute phase. Rest and stress perfusion in combination with late Gadolinium enhancement can provide information about the clinical significance of perfusion defects in the area supplied by the involved coronary artery.

Myocardial perfusion by CMR

First-pass perfusion CMR has recently emerged as a reliable and non-invasive technique for the detection of myocardial ischemia in adult ischaemic heart disease. According to a recent large clinical trial, CMR has proven to be a safe alternative to SPECT to detect perfusion deficits in adult ischaemic heart disease [23].

In patients with chronic KD, the AHA recommends echocardiography for routine follow up, nuclear perfusion scans for the detection of inducible ischemia and conventional coronary angiography in selected patients [2]. However, CMR perfusion can be used as an alternative technique and has been used for the long-term evaluation of KD [24, 25] (Fig. 9). Protocols for the acquisition of first-pass adenosine stress perfusion CMR need to be adapted to the specific needs of infants and children who are either sedated or under general anaesthesia. Higher spatial resolution is needed, as well as faster acquisition times due to higher heart rates.

Fig. 9. The 3 year old patient with a giant aneurysm shown in Fig. 4 in the left main and proximal left anterior descending.

Fig. 9

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The left circumflex comes of the distal end of the giant coronary aneurysm. A perfusion defect is clearly seen under Adenosine perfusion (140mcg/ kg/min; (b) compared to rest conditions (a). kt-blast SSFP, spatial resolution 1.7 × 1.9.10 mm, TR/TE 2.8/1.4 ms, flip angle 50°, saturation prepulse with saturation delay 100 ms, kt factor 5 with 11 training profiles. G. F. Greil, KCL London

Advantages of CMR perfusion over the competing techniques, include the absence of ionizing radiation; the ability to add a comprehensive CMR functional examination; the excellent safety profile of the contrast agents currently used and superior spatial resolution [23, 55]. However, data about stress perfusion in KD are limited [39]. Whilst there are a number of advances that may add to the reliability of CMR perfusion in smaller children, currently there is not enough information regarding its utility or repeatability. Therefore, further multi-center studies are needed in order to establish the clinical utility of stress perfusion CMR in KD.

Contra-indications and issues of safety

The gadolinium contrast agents currently used for perfusion, viability and angiography evaluation, have very low nephrotoxicity, but some agents have been linked to systemic fibrosis in patients with renal failure, (nephrogenic systemic fibrosis (NSF)). NSF is a very rare complication, although there is no exact estimation of its prevalence in the literature. It provokes fibrosis of the skin and connective tissue, leading to contractures and joint immobility. In a later phase, it can also involve other organs such as lungs, liver, heart and finally lead to death. According to our knowledge, NSF occurred only in patients with severe renal dysfunction, typically with a glomerular filtration rate of <30 ml/min/1.73 m2. Effective treatment of NSF is not available to date [56]. Moreover, no cases of NSF have been reported since the administration of gadolinium based contrast agents was regulated in patients with renal dysfunction. There are only scarce data about the safety of contrast agent for heart studies in children. According to a recent study, CMR and MRA can be accomplished safely in neonates and infants ≤120 days old for a wide range of pre-surgical cardiac indications. Adverse events were unrelated to patient age, complexity of heart disease, type of anesthesia or PGE1 dependence [56]. Otherwise, the usual MRI contraindications for patients with metallic implants apply [57].

CMR challenges: what’s new?

Perfusion

CMR perfusion allows the visualization of the wash-in of Gadolinium in the myocardium during adenosine infusion and at rest. The high temporal resolution required to visualize the first-pass of the contrast agent is the main limiting step to the achievable spatial resolution, which is usually lower compared with coronary, functional and late gadolinium enhancement imaging. New acquisition strategies such as k-space and time sensitivity encoding (kt SENSE), allow for substantial acceleration of data acquisition [58]. This speed enables an improvement in spatial resolution with a favourable signal to noise ratio particularly at three Tesla [59]. In practice, the higher spatial resolution allows a reduction of the incidence and severity of dark rim artefacts; the assessment of the presence of subendocardial ischemia and the assessment of gradients of transmural perfusion [60, 61]. This increased spatial resolution is vital for children because the left ventricular wall thickness is lower than adults and we would presume that might preclude a satisfactory evaluation using any other modality (e.g. nuclear medicine techniques). Moreover, the high spatial resolution may potentially also permit the assessment of perfusion of the thin-walled RV myocardium, previously not measurable by perfusion-CMR [60]. Currently data about the application of kt-SENSE in children is still missing.

Tissue characterization

Sophisticated techniques providing detailed information about diffuse oedema and fibrosis are now available. Quantitative T2 mapping identifies myocardial oedema without the limitations encountered by T2-W short tau inversion recovery imaging [62] and could offer the potential for increased accuracy in the detection of myocardial oedema [63]. Additionally, the application of T1 mapping, that has been recently used to identify diffuse fibrosis in heart failure, may offer a quantitative approach in microfibrosis assessment commonly found during the course of myocardial inflammation and heart failure during KD [64].

Whole body MRA

Another important question in the follow up of KD is the evaluation of other arteries that can be also involved during the course of the disease. The application of whole-body MRA screening has already been used in adult ischaemic heart disease [65] and it may therefore also allow previously unknown concomitant vascular disease to be detected in KD patients.

Plaque evaluation

Previous studies have demonstrated that carotid plaque contrast enhancement on MRI correlates with inflammatory cell infiltration at histopathology [66]. Once the technical problems such as compensation for cardiac and respiratory motion are solved, this technology could be transferred to give additional information about CAA pathophysiology during the follow up of KD.

Higher field strength

In some applications, the clinical use of cardiac MRI has begun to move towards 3T. Particularly when contrast agents are used, such as in first pass perfusion and late Gadolinium enhancement imaging [67], higher field strengths improve image quality. Coronary artery lumen and vessel wall imaging may also benefit from higher field strength to achieve higher spatial resolution but several technical challenges have to be overcome. Recently, it has been demonstrated that wideband SSFP has the ability to achieve sub-millimeter resolution whilst avoiding banding artefacts that confound the use of conventional balanced SSFP at 3T. This approach provides roughly 25 % higher SNR efficiency compared to balanced SSFP at 1.5T making it a promising candidate for non-contrast coronary MRA at 3T [68, 69]. Other approaches to improve image quality of 3T coronary MRA have been investigated including the use of contrast agents [70]. As previously described, the underlying standard sequence employs navigators for respiratory motion compensation and T2-preparation for adequate suppression of signal from the myocardium. ECG gating either in systole or diastole may further improve image quality [71].

New contrast agents

The application of novel contrast agents is very difficult particularly in children as safety has absolute priority. Therefore only its potential use will be outlined in this section. Immune cell infiltration by mainly macrophages and monocytes, has been identified with CMR using ultrasmall super-paramagnetic-iron-oxide (USPIO). Recently, viable and nonviable peri-infarction regions of the myocardium after ischemia were differentiated with great accuracy using USPIO [72]. This technique may also be useful for the identification of allograft rejection after heart transplantation [73] and for vessel remodelling [74]. This latter use may therefore be of potential value for the evaluation of KD.

Diagnostic algorithm

The rapid evolution of CMR allows non-invasive, radiation-free evaluation of coronary anatomy, coronary wall, myocardial inflammation, stress myocardial perfusion and myocardial fibrosis during one single examination. One of the remaining challenges is the lack of both single and multi-center studies in KD to prove the benefits of CMR in the better management of these patients. There is a need for further reduced acquisition time to improve patient comfort and reduce CMR cost.

A CMR diagnostic algorithm for KD risk level IV–V is proposed in Table 2.

Table 2. CMR diagnostic algorithm for KD risk levels III-V.

Type of CMR evaluation Acute phase Chronic phase
Coronary artery lumen Recommended Recommended
Coronary artery vessel wall Under investigation Under investigation
Myocardial function Recommended Recommended
Myocardial inflammation Under investigation Not recommended
Rest myocardial perfusion Under investigation Only as a part of stress perfusion
Stress myocardial perfusion Under investigation Recommended. Standard contraindication to stress perfusion apply*
Myocardial fibrosis assessment Recommended Recommended
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Contraindications to CMR stress perfusion: Myocardial infarction <3 days, unstable angina pectoris, severe arterial hypertension, asthma or severe obstructive pulmonary disease requiring treatment, atrio-ventricular block >IIa, trifascicular block, allergy against adenosine, allergy against gadolinium-based contrast agents or renal insufficiency, other contraindications for adenosine or dipyridamole. Adenosine must be administered with caution in patients with autonomic nerve dysfunction, stenotic valvular disease, cerebrovascular insufficiency, any obstructive lung disease, co-medication with beta-blockers, Ca-antagonists or cardiac glycosides (due to AV/sinus node depression) (From Chiribiri A, Plein, S, Nagel E. Perfusion stress MR, in Kramer CM, Hundley WG. Atlas of Cardiovascular Magnetic Resonance Imaging: An Imaging Companion to Braunwald’s Heart Disease. Saunders 2009)

Conclusions

KD is an autoimmune systemic disease involving coronary and peripheral vessels, pericardium and all layers of the myocardium. The early application of immunoglobulin has modified the phenotypic expression of KD. However, CAAs, myocardial inflammation and myocardial infarction continue to present as life-threatening complications of this disease [4]. CMR can offer a detailed evaluation of the coronary lumen and vessel wall, myocardial perfusion, ventricular function, myocardial inflammation and fibrosis. The development of new CMR sequence technology and hardware will provide better image quality with faster data acquisition and will allow a better understanding of KD pathophysiology.

Acknowledgments

The Division of Imaging Sciences receives support from the Centre of Excellence in Medical Engineering (funded by the Wellcome Trust and the Engineering and Physical Sciences Research Council; grant WT 088641/Z/09/Z) as well as the British Heart Foundation Centre of Excellence (British Heart Foundation award RE/08/03). Further support is provided through the Medical Research Council (MRC) Centre for Transplantation, King’s College London, UK (MRC grant no. MR/J006742/1). This research was also supported by the National Institute for Health Research (NIHR) Biomedical Research Centre at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. The authors thank James Otton, St Vincent’s Hospital Sydney, Australia, for his comments regarding the use of Computed Tomography for coronary imaging.

Footnotes

Conflict of interest There is no conflict of Interest for any of authors of the review.

1

Kim and Goo [75].

Contributor Information

George Papadopoulos, Aglaia Kyriakou Children’s Hospital, Athens, Greece.

Tarique Hussain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London, SE1 7EH, UK; Department of Paediatric Cardiology, Evelina Children’s Hospital, London, SE1 7EH, UK.

Amedeo Chiribiri, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London, SE1 7EH, UK.

Rene Botnar, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London, SE1 7EH, UK.

Gerald F. Greil, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London, SE1 7EH, UK Department of Paediatric Cardiology, Evelina Children’s Hospital, London, SE1 7EH, UK.

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