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DOI:10.2214/AJR.05.1414
AJR 2007; 188:W534-W539
© American Roentgen Ray Society

Clinical Observations

Utility of Coronary MR Angiography in Children with Kawasaki Disease

Atsushi Takemura1, Atsuko Suzuki2, Rikako Inaba2, Tomoyoshi Sonobe3, Keiji Tsuchiya3, Masami Omuro1 and Tateo Korenaga1

1 Department of Radiology, Tokyo Postal Services Agency Hospital, Chiyoda-ku, Fujimi 2-chome, 14-23, Tokyo, Japan 102-8798.
2 Department of Pediatrics, Tokyo Postal Services Agency Hospital, Tokyo, Japan.
3 Department of Pediatrics, Japan Red-Cross Medical Center, Tokyo, Japan.

Received August 13, 2005; accepted after revision August 18, 2006.

 
Address correspondence to A. Takemura (atsu-papa{at}mm.em-net.ne.jp).

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Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. Although coronary arterial lesions due to Kawasaki disease (KD) should be evaluated as early as possible after the acute phase, conventional X-ray coronary angiography poses high risks for young children with the disease. The use of noninvasive MR coronary angiography is desirable, although it is difficult to produce clear images in young children. We developed a method to improve the quality of MR coronary angiography in young children. MR coronary angiography with vector electrocardiogram gating, real-time navigator-echo, 3D, steady-state free precession was performed in 35 children with KD. Many parameters (i.e., field of view, acquisition delay, turbo-field echo-factor, navigator window, and resolution) were optimized for each patient.

CONCLUSION. Optimization resulted in the acquisition of high-resolution and highsignal images of the coronary arteries. It remarkably improved not only the quality of the images, but also the detection rate of coronary artery segments. MR coronary angiography is a useful method for evaluating coronary aneurysms from the early stages of KD, even in infants and small children.

Keywords: coronary aneurysm • Kawasaki disease • MR coronary angiography • pediatric imaging • whole-heart imaging


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Coronary aneurysms due to Kawasaki disease (KD) decrease in size soon after the acute phase, which is defined as the first 30 days of illness. Evaluation of aneurysmal size is necessary for risk stratification and therapeutic management as soon as possible after the acute phase. Furthermore, aneurysms often progress to obstructive lesions in the late stage of KD [1]. Therefore, patients with aneurysms after KD need follow-up with coronary angiography (CAG) throughout their lives.

Most patients with KD are infants and children younger than 4 years [2], and CAG often entails risk for such young children. The risks include worsening of the anemia of KD due to bleeding from a punctured femoral artery; thrombotic occlusion of the femoral artery due to puncture of a postinflammatory vessel in the hypercoagulable state, which continues more than 1 year after KD [3]; and myocardial infarction, which sometimes occurs during or after CAG. The considerable radiation exposure of frequent CAG also is a serious problem for young children. These risks indicate the need for a noninvasive simple method of evaluating coronary aneurysms.

Although the usefulness of MR CAG in adults is well known [4, 5], the effectiveness of this technique in infants is not well established. Moreover, to our knowledge, there have been no reports of MR CAG performed on infants. The procedure is difficult because infants have a narrow coronary artery (1–2 mm in diameter) and a fast heart rate (80–130 beats/min) and cannot hold their breath during the examination. However, the development of a new respiratory gating technique (navigator echo) [6] whereby MR CAG can be performed with the patient breathing freely has led to the possibility of visualizing the coronary arteries of infants. We studied the utility of MR CAG in visualizing coronary arterial lesions in patients younger than 6 years with KD. We used cardiac gating and real-time navigator echo technique with radial k-space sampling and a 3D steady-state free precession (SSFP) MRI sequence [7–9].


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
This retrospective study included 35 patients younger than 6 years who underwent MR CAG between September 2003 and December 2004. These children were undergoing follow-up because a transient dilated lesion had been found during the acute phase of KD or coronary arterial lesions had been found as sequelae of KD. The patients were 10 girls and 25 boys with an age range of 8 months to 6 years 7 months (median age, 3 years 7 months). The heart rate range was 70–127 beats per minute (BPM) (mean ± SD, 103 ± 14 BPM), and the body weight range was 5.6–22.6 kg (mean weight, 12.9 ± 4 kg).


Figure 1
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  		Fig. 1 —Graph shows rate of visualization of each segment of coronary artery (n = 35). LCX = left circumflex branch, LAD = left anterior descending branch, LMT = left main trunk, RCA = right coronary artery.

 
All patients were given sodium trichloroethylene phosphate syrup (0.8–1.0 mL/kg) so that they could sleep during the imaging examination. If the syrup was not effective, we administered thiopental sodium (2–5 mg/kg) by IV infusion. The interval between MR CAG and cardiac sonography for the 35 patients was 0–90 days (median, 6 days). Five patients had undergone CAG follow-up, and the interval between CAG and MR CAG was 5–240 days (median, 60 days). Written informed consent was obtained from the parents of all participants before each MR CAG examination. The study was approved by the committee on clinical investigations at our hospital.

Imaging
All studies were performed with a 1.5-T whole-body fast-gradient (maximum gradient, 30 mT/m; maximum slew rate, 150 mT/m/ms) MRI system (Gyroscan Intera Master Gradient, Philips Medical Systems) equipped with cardiac software. Because of the small body size of infants, a two-element flex-medium coil (Flex-M, Philips Medical Systems) was used instead of a five-element synergy cardiac coil for signal reception. The Flex-M coil is a set of two oval receiver coils with an external diameter of 170 x 200 mm. One coil was set on the chest and the other on the back [10].

Three-dimensional SSFP with vectorcardiographic real-time navigator echo technique was used to visualize the coronary arteries without contrast material. Two methods were used for slice positioning. Three-point-plan scanning [11] was used for 20 patients, and whole-heart imaging [12] was used for 15 patients. The images were reconstructed into maximum-intensity-projection, curved multiplanar reformation, soap-bubble maximum-intensity-projection (Philips Medical Systems), and volume-rendered (M900 Quadra system, Ziosoft) images. For three-point-plan scanning and whole-heart imaging, the diastolic rest period was defined through identification of the heart movement of each patient with 2D SSFP retrospective cine MRI with vectorcardiography. Classification of the coronary arteries into American Heart Association segments [13] increased the visualization rate. The targeted segments evaluated were the right coronary artery (segments 1–4), left main trunk (segment 5), left anterior descending branch (segments 6–10), and the left circumflex branch (segments 11–15).

Three-point-plan scanning and whole-heart imaging—Navigator gating with prospective slice correction was used to compensate for respiratory motion. A flow-insensitive T2-weighted preparatory pulse [14] for contrast enhancement without the use of contrast material was followed by a localized anterior saturation preparatory pulse, navigator echo, a spectrally selective fat-saturation pulse (spectral presaturation by inversion recovery), and a 3D segmented k-space gradient-echo sequence (TR range/TE range, 4.3–5.0/2.2–2.5; flip angle range, 90–100°; radial k-space sampling technique). These sequences were followed by three-point-plan scanning and whole-heart imaging with eight phase-encoding steps per cardiac cycle, so-called bright-blood imaging. Data were acquired along the major axis of the artery. Flow-compensating gradients were not used. Slices 1.8 mm thick (interpolated to 0.6 mm) were acquired with a 180- to 200-mm field of view and were reconstructed with a 512 x 360 matrix (in-plane voxel size, 0.35 x 0.35 mm). The parallel imaging technique of sensitivity encoding [15] was used, usually with accelerator factors 1.3 in the phase direction and 1.0 in the slice direction.

Cine MRI—An ECG-triggered turbo field-echo SSFP cine MRI sequence (one signal acquired per R-R interval; heart rate phase, 80; cardiac synchronization, retrospective gating) was applied in the transverse plane at the level of the proximal to medial right coronary artery for visual determination of the optimal diastolic rest period. The sequence parameters were as follows: 4.2/1.88; flip angle, 60°; field of view, 220 mm. A 192 x 154 matrix with cartesian k-space sampling yielded an in-plane resolution of approximately 1.15 x 0.87 mm (reconstructed 256 x 256 matrix, 0.8 x 0.8 mm).

Slice positioning technique: three-point-plan scanning, whole-heart imaging, and cine MRI— For three-point-plan scanning, the axial image was used to determine the imaging plane for one targeted artery. Three points were plotted on the targeted artery, and the computer was used to calculate the position of the scanning plane. Twenty to 30 slices were used, and the scanning time was approximately 3–5 minutes for four sections: three sections for visualization of the right coronary artery, left main trunk, left anterior descending branch and left circumflex branch and one section for visualization of the root of the left main trunk, left anterior descending branch, and left circumflex branch simultaneously. Thus, the overall scanning time was approximately 15–30 minutes. For whole-heart imaging, 130–150 axial slices covered the entire heart. Because this technique covers the entire heart at once, one section is imaged in approximately 20–30 minutes.

With reference to the coronal image of the survey scan, the axial plane for cine MRI was set to the center of the heart. After the heart phase of the patient was defined, the scan was started. Because the patient was asleep, the scan was obtained under normal respiration. The short-axis image of the right coronary artery was obtained, and by evaluation of the diastolic rest period of phase 80, the trigger-delay program was set to acquire the data for three-point-plan scanning or whole-heart imaging.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The imaging examination was successful for 34 of the 35 patients, a success rate of 97%. The 35th patient was wearing an undershirt with a metallic zipper that had not been noticed. Among 525 segments, 313 (60%) were evaluated. The visualization rate of the coronary arteries was 97% for segment 1, 97% for segment 2, 89% for segment 3, and 57% for segment 4 in the right coronary artery; 97% for segment 5 in the left main trunk; 97% for segment 6, 86% for segment 7, 43% for segment 8, 8.6% for segment 9, and 5.7% for segment 10 in the left anterior descending branch; and 91% for segment 11, 5.7% for segment 12, 54% for segment 13, 34% for segment 14, and 31% for segment 15 in the left circumflex branch (Fig. 1). Comparison of the visualization rate of the peripheral coronary arteries (segments 4, 7, 8, and 12–15) with three-point-plan scanning and whole-heart imaging indicated that the rate of visualization with whole-heart imaging (54.4%) was greater than that with three-point-plan scanning (35.8%) (p < 0.01). The rate of visualization of the dilated coronary arterial lesions of 18 segments in 12 coronary arterial lesions had a sensitivity of 94.7%, specificity of 98.8%, positive predictive value of 94.7%, negative predictive value of 98.8%, and accuracy of 98.1%.


Figure 2
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  		Fig. 2A —1-year-5-month-old boy with Kawasaki disease. Ao = aorta. MR coronary angiograms obtained with cardiac coil made for adults while disease is in acute stage shows left anterior descending branch (arrow, A), left circumflex branch (arrowhead), and aneurysm at bifurcation of left coronary artery (triangle). Although aneurysm is evident, image is not clear.

 


Figure 3
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  		Fig. 2B —1-year-5-month-old boy with Kawasaki disease. Ao = aorta. MR coronary angiograms obtained with cardiac coil made for adults while disease is in acute stage shows left anterior descending branch (arrow, A), left circumflex branch (arrowhead), and aneurysm at bifurcation of left coronary artery (triangle). Although aneurysm is evident, image is not clear.

 


Figure 4
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  		Fig. 2C —1-year-5-month-old boy with Kawasaki disease. Ao = aorta. MR coronary angiograms obtained with Flex-M coil (Philips Medical Systems) while disease is in convalescent stage shows left anterior descending branch (arrow, C), and left circumflex branch (arrowhead). Regression of aneurysm was verified. Image is clear and shrinkage of aneurysm is evident.

 


Figure 5
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  		Fig. 2D —1-year-5-month-old boy with Kawasaki disease. Ao = aorta. MR coronary angiograms obtained with Flex-M coil (Philips Medical Systems) while disease is in convalescent stage shows left anterior descending branch (arrow, C), and left circumflex branch (arrowhead). Regression of aneurysm was verified. Image is clear and shrinkage of aneurysm is evident.

 
Patient 1 was a boy 1 year 5 months old who weighed 8.8 kg and had a heart rate of 105 BPM. MR CAG with a synergy cardiac coil performed on the 21st day of illness (Figs. 2A and 2B) depicted an aneurysm at the root of the left circumflex branch of the left coronary artery. The peripheral coronary arteries of the left anterior descending branch and the left circumflex branch also were identified. However, the spatial resolution of the image was low, so the image was not clear. To verify regression of the aneurysm after an interval of 3 months, MR CAG was repeated with a Flex-M coil (Philips Medical Systems), and regression was clearly visualized (Figs. 2C and 2D). Moreover, image quality improved because of a high signal-to-noise ratio, and the left circumflex branch was clearly visualized.

Patient 2 was a boy 3 years 11 months old who weighed 15.3 kg and had a heart rate of 113 BPM. CAG was performed because of giant coronary aneurysms on the left coronary artery (segments 5–7), right coronary artery (segments 1–4), and left circumflex branch (segment 11) (Figs. 3A and 3B). MR CAG was performed 3 days later, on the 90th day of illness (Figs. 3C, 3D, 3E, 3F, 3G, 3H). The giant coronary aneurysms were clearly visualized with MR CAG, the findings of which showed excellent agreement with the CAG findings.


Figure 6
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  		Fig. 3A —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Coronary angiogram of right coronary artery shows aneurysm (triangles).

 

Figure 7
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  		Fig. 3B —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Coronary angiogram of left coronary artery shows aneurysms of left anterior descending branch (arrow) and left circumflex branch (arrowhead).

 

Figure 8
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  		Fig. 3C —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Maximum-intensity-projection whole-heart coronary angiogram obtained 3 days after A and B shows aneurysm (triangles) on right coronary artery. Ao = aorta.

 

Figure 9
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  		Fig. 3D —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Maximum-intensity-projection whole-heart coronary angiogram obtained in same examination as C shows left anterior descending branch (arrow). Ao = aorta.

 

Figure 10
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  		Fig. 3E —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Maximum-intensity-projection whole-heart coronary angiogram obtained in same examination as C and D shows left circumflex branch (arrowhead). Ao = aorta.

 

Figure 11
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  		Fig. 3F —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Soap-bubble maximum-intensity-projection image shows all three branches in one plane. Triangle indicates right coronary artery; arrow, left anterior descending branch; arrowhead, left circumflex branch. Ao = aorta.

 

Figure 12
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  		Fig. 3G —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Reconstructed volume-rendered images (G, whole heart; H, heart removed and remaining coronary arteries) show aneurysms at segment 1 in right coronary artery (triangles), left anterior descending artery (arrow), and left circumflex artery (arrowhead).

 

Figure 13
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  		Fig. 3H —3-year-11-month-old boy with Kawasaki disease and giant coronary aneurysms of segments 1–7 and 11. Reconstructed volume-rendered images (G, whole heart; H, heart removed and remaining coronary arteries) show aneurysms at segment 1 in right coronary artery (triangles), left anterior descending artery (arrow), and left circumflex artery (arrowhead).

 
Patient 3 was a boy 5 years 7 months old who weighed 16.6 kg and had a heart rate of 70 BPM. MR CAG was performed 47 months after the onset of KD. A dilated lesion on the left coronary artery (segment 6) was visualized clearly with all methods of MRI (Fig. 4A, 4B, 4C, 4D).


Figure 14
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  		Fig. 4A —5-year-7-month-old boy with Kawasaki disease. Dilated lesion (arrow) was visualized on left anterior descending branch (segment 6) on all reconstructed images. Coronal oblique (A) and axial oblique (B) maximum-intensity-projection images. Ao = aorta.

 

Figure 15
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  		Fig. 4B —5-year-7-month-old boy with Kawasaki disease. Dilated lesion (arrow) was visualized on left anterior descending branch (segment 6) on all reconstructed images. Coronal oblique (A) and axial oblique (B) maximum-intensity-projection images. Ao = aorta.

 

Figure 16
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  		Fig. 4C —5-year-7-month-old boy with Kawasaki disease. Dilated lesion (arrow) was visualized on left anterior descending branch (segment 6) on all reconstructed images. Soap-bubble maximum-intensity-projection image. Ao = aorta.

 

Figure 17
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  		Fig. 4D —5-year-7-month-old boy with Kawasaki disease. Dilated lesion (arrow) was visualized on left anterior descending branch (segment 6) on all reconstructed images. Volume-rendered image.

 

Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
KD has an unknown origin, and it usually occurs in infants and children younger than 4 years [11]. In Japanese patients, coronary aneurysms develop in the acute phase in 16% of patients and remain in 5% as a sequela after the convalescent phase. These aneurysms decrease in size soon after the acute stage and often regress completely within 2 years, but some develop to occlusion or localized stenosis of the artery even 10 or 20 years after the onset of the disease [1]. To predict the progress of the disease and determine appropriate treatment and follow-up protocols, it is essential to understand the size and shape of the aneurysms in the early phase. Therefore, invasive CAG should be performed as soon as possible after the acute stage [2]. However, CAG poses high risk to young children with KD. Furthermore, patients need follow-up with frequent CAG throughout their lives. A noninvasive method of visualizing aneurysms immediately after the acute phase, and thrombus and the coronary arteries during follow-up, has long been needed.

We have been performing noninvasive coronary artery imaging with MRI since 2000 and have conducted follow-up of the coronary arteries of patients with KD [9, 16]. At first we used 3D fast low-angle shot [17] and 3D magnetization-prepared rapid acquisition gradient-echo imaging [18–20] with contrast agents and with breath-hold (30 seconds) to image the coronary artery. Later we were able to image the coronary arteries without contrast agents by using the true fast imaging with SSFP sequence [21]. This examination, however, is not suitable for infants and young children, who cannot hold their breath for imaging. However, with the invention of the navigator echo technique, coronary artery imaging can be performed during free breathing [6, 9].

Although there are many reports of MR CAG of adults [4–7, 22], to our knowledge there have been no reports, except for those by our group [7, 8, 15, 16], of MR CAG of infants. We have performed MR CAG on more than 200 patients with coronary artery lesions due to KD. It is very difficult, however, to visualize the coronary arteries of young children compared with those of adults. We have optimized the receiver coils and the exact data acquisition technique to improve the visualization rate of MR CAG of infants and children.

Children younger than 6 years have small bodies and narrow coronary arteries. It became clear that the cardiac coil we were using was not suitable for these children. Image turbulence occurred because the coil did not maintain high spatial resolution. In contrast, the Flex-M coil is suitable for small children and improved visualization of the coronary artery with high spatial resolution and a high signal-to-noise ratio. Head coils or knee coils previously were used to image the thorax and abdomen of young children. Because these are single coils, we could not perform parallel imaging. It is well known that parallel imaging can be effective in many ways, such as coil sensitivity correction, reduction of scanning time, and high-resolution imaging [17]. We therefore used the Flex-M coil for parallel imaging to maintain spatial and time resolution and succeeded in improving visualization of the coronary arteries in children.

In infants, the heart and coronary arteries are small, the heart rate is high, and the heart is moving at all times. To image the coronary arteries accurately under these conditions, it is important to set the vectorcardiographic gating parameters exactly so that blurring induced by heartbeats is minimized and excellent images are obtained. To identify motion of the heart, we performed retrospective cine MRI (50–80 phases). We then tried to acquire data during the diastolic rest period with cine MRI. We were able to obtain coronary artery images as high-resolution 3D data by collecting the data only at the expiration position without breath-hold. The navigator echo technique conventionally allows extension of scanning time, which is why breath-hold scans are widely used. However, with the invention of parallel imaging, it has become possible to reduce scanning time, and the navigator echo technique has become the more widely used coronary artery imaging technique. Because breath-hold is not necessary with this technique, it was possible to perform MR CAG on the children in our study. Moreover, with correct setting of the parameters, the coronary arteries were visualized in children with heart rates greater than 100 BPM. The examination success rate was 97%.

Because 3D volume data on the entire heart are obtained as CT images in whole-heart imaging, the data from any section or direction can be reconstructed and visualized. Moreover, the rate of visualization of the peripheral coronary arteries in children is better with whole-heart imaging than with three-point-plan scanning.

If several techniques are used, it is possible to obtain high-resolution coronary artery images as 3D whole-heart images with SSFP. The techniques can be performed noninvasively without contrast enhancement and without a breath-hold. The images obtained can be reconstructed and every section of the coronary arteries visualized, which is impossible with CAG. MR CAG is a useful method of evaluating coronary arterial lesions in children with KD, even those younger than 6 years.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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