DOI: 10.1148/radiol.2442061045
(Radiology 2007;244:399-410.)
© RSNA, 2007
Juvenile and Adult Congenital Heart Disease: Time-resolved 3D Contrast-enhanced MR Angiography1
Michael Fenchel, MD,
Roya Saleh, MD,
Howard Dinh, MD,
Margaret H. Lee, MD,
Kambiz Nael, MD,
Mayil Krishnam, MD,
Stefan G. Ruehm, MD, PhD,
Stephan Miller, MD,
John Child, MD, and
J. Paul Finn, MD
1 From the Department of Diagnostic Radiology, Eberhard-Karls-University, Hoppe-Seyler-Str 3, 72076 Tuebingen, Germany (M.F., S.M.); and Departments of Radiological Sciences (M.F., R.S., M.H.L., K.N., M.K., S.G.R., J.P.F.) and Medicine (H.D., J.C., J.P.F.), David Geffen School of Medicine, University of California Los Angeles, Los Angeles, Calif. Received June 16, 2006; revision requested August 21; revision received September 19; accepted October 26; final version accepted December 22. M.F. supported by a research grant from the Deutsche Forschungsgemeinschaft (#FE 610/4-1).
Address correspondence to M.F. (e-mail: michael.fenchel{at}med.uni-tuebingen.de).
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ABSTRACT
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Purpose: To assess the incremental diagnostic value of time-resolved three-dimensional (3D) magnetic resonance (MR) angiography over single-phase 3D MR angiography and cine MR imaging in juvenile and adult patients with congenital heart disease (CHD).
Materials and Methods: The study was HIPAA compliant and was approved by the institutional review board. Written informed consent was obtained from each patient. Eighty-one consecutive patients (46 male and 35 female patients; mean age, 31.1 years ± 13.5 [standard deviation]) with CHD were examined with a 1.5-T MR imaging unit. The imaging protocol comprised time-resolved MR angiography (repetition time msec/echo time msec, 2.01/0.81) after injection of 0.03 mmol gadodiamide per kilogram of body weight at 4 mL/sec and single-phase high-spatial-resolution MR angiography (2.87/0.97) after injection of 0.15 mmol/kg gadodiamide at 1.5 mL/sec. After review of the time-resolved and conventional MR angiographic data sets, each of two independent observers listed the additional clinical information gained from time-resolved MR angiographic data. A Wilcoxon signed rank test was used to test for statistical differences between the image quality ratings of the two observers.
Results: Time-resolved and single-phase high-spatial-resolution MR angiography yielded diagnostic image data in all patients. Observers 1 and 2 found functional information in time-resolved MR angiographic series in 52 and 51 patients, respectively, that was not seen at high-spatial-resolution MR angiography. Intra- and extracardiac shunts, respectively, were exclusively depicted by time-resolved MR angiography for observer 1 in 18 and two patients and for observer 2 in 15 and two patients. However, both observers reported higher confidence in the assessment of such smaller vascular structures as supraaortic vessels (in 12 patients for observer 1 and 11 patients for observer 2) and major aortopulmonary collateral arteries (in eight patients for observer 1 and 10 patients for observer 2) at high-spatial-resolution MR angiography. No significant difference was evident in image quality scoring between the two observers (P = .32 for time-resolved and P = .47 for conventional MR angiography).
Conclusion: Compared with conventional MR angiography, time-resolved MR angiography yields clinically relevant information in a substantial number of patients; hence, the two techniques should be regarded as complementary.
© RSNA, 2007
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INTRODUCTION
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With the improvement of various surgical and interventional techniques, more than 85% of infants with congenital heart disease (CHD) now reach adulthood in developed countries (1,2). Therefore, it is not surprising that today about 1 million adult Americans live with CHD (3). Because residua, sequelae, and postsurgical complications determine the long-term outcome of corrected or palliated CHD (4), timely detection and quantification of morphologic and functional abnormalities require accurate and, preferably, noninvasive imaging methods. Echocardiography is the most frequently used noninvasive technique for studying cardiac morphology and function and provides fast and accurate information in neonates, infants, and young children. However, in older patients, particularly those with complex or treated malformations, acoustic access with transthoracic echocardiography may be limited by scar tissue, bone, lung tissue, or chest wall deformity.
Conventional angiography is regarded as the reference standard for evaluation of cardiac and vascular anatomy, and important information about intracardiac pressures, pulmonary vascular resistance, and oxygen saturation can be obtained in no other way. Nevertheless, catheterization has a known complication rate, and conventional angiography requires the use of ionizing radiation and intravenous iodinated contrast agents, which are undesirable for repeated applications. Magnetic resonance (MR) imaging and MR angiography have become widely accepted in the diagnosis of vascular disease—for example, stenosis, aneurysm, and occlusion—over the past several years (5–9). However, dynamic changes seen in intra- or extracardiac shunts or postsurgical leaks may not be defined at conventional (non–time-resolved) MR angiography, where temporal acquisition windows are on the order of 20 seconds or more. Furthermore, at conventional MR angiography, structures in the right and left sides of the heart are often enhanced simultaneously, mandating the use of multiplanar reconstructions to "untangle" overlapping vessels (10,11).
More recently, time-resolved contrast material–enhanced techniques have been introduced and suggested for functional and anatomic assessment of abnormalities of the thoracic, abdominal, and peripheral blood vessels (12–14). By combining information about vascular anatomy with information about flow directionality, these methods become especially suitable for detection and follow-up of the complex hemodynamic findings in many patients with CHD and postsurgical changes. By clarifying the sequence of vascular and chamber enhancement in a visually intuitive way, time-resolved MR angiography has the potential to simplify the interpretation of single-phase MR angiographic studies and to provide additional information about functional cardiovascular anatomy.
Thus, the aim of our study was to assess the incremental diagnostic value of time-resolved three-dimensional (3D) MR angiography over single-phase 3D MR angiography and cine MR imaging in juvenile and adult patients with CHD.
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MATERIALS AND METHODS
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Our study was not directly supported by industry, although our institution has a research collaboration with Siemens Medical Solutions, Malvern, Pa. Data and information submitted for publication were under the control of those authors who are not employees of Siemens Medical Solutions.
Patients
Between August 2004 and November 2005, 81 consecutive juvenile (n = 13; age range, 12–18 years) and adult (n = 68; age range, 19–70 years) patients (46 male patients, 35 female patients; mean age, 31.1 years ± 13.5) with CHD who were referred for MR imaging were enrolled in the study. Inclusion of patients was based on ability and willingness to participate in the study, as well as a lack of contraindications to MR imaging. Our study was approved by the institutional review board of University of California Los Angeles, and informed consent was obtained from all participants or their parents or legal caretakers. Our study was Health Insurance Portability and Accountability Act compliant. All examinations were performed at the University of California Los Angeles. Primary diagnoses in the patients were varied (Table 1), and 65 of the patients had undergone previous surgery for palliative or definitive correction of CHD (Table 2).
MR Imaging Protocol
All examinations were performed with a 32-channel 1.5-T MR imaging unit (Magnetom Avanto; Siemens Medical Solutions) with a maximum gradient amplitude of 45 mT/m and a maximum slew rate of 200 (mT·m–1)/msec along each physical axis. Individuals were examined in the supine position; for signal reception, phased-array multielement surface coils were used.
Prior to the examination, a 20-gauge intravenous catheter was placed in an antecubital vein to facilitate contrast medium injection. Multiplanar scout images were obtained with single-shot steady-state free precession (SSFP). The examination protocol comprised the acquisition of breath-hold SSFP cine images (15) (repetition time msec/echo time msec, 2.4/1.2; flip angle, 65°; bandwidth, 975 Hz/pixel; matrix, 200 x 256; field of view, 260 x 320 mm2; section thickness, 6 mm; temporal resolution, 40.3 msec) in the cardiac short axis and vertical and horizontal long axes, as well as in several nonstandardized orientations depending on the patient's underlying anatomic status. Furthermore, velocity-encoded cine MR imaging (9.6/2.6; flip angle, 25°; bandwidth, 500 Hz/pixel; matrix, 80 x 256; field of view, 188 x 300 mm2; section thickness, 6 mm; temporal resolution, 58 msec) was performed as deemed appropriate by the supervising physician. Two supervising physicians (J.P.F., with 20 years of experience with MR angiography, and S.G.R., with 12 years of experience) were involved in the study.
Time-resolved MR imaging.—The time-resolved 3D MR angiography sequence was a coronal spoiled gradient-recalled echo acquisition (12) performed with the following parameters: 2.01/0.81; flip angle, 20°; bandwidth, 1120 Hz/pixel; field of view, 400 x 480 mm2; matrix, 256 x 384; voxel size, 1.6 x 1.3 x 7.0 mm3; generalized autocalibrating partially parallel acquisition (16) factor, two; number of partitions, 14; temporal resolution, 2.3 seconds (interpolated with time-resolved echo-shared angiographic technique [TREAT] to 1.5 seconds over a 23-second acquisition window). Images were acquired after injection of 0.03 mmol gadodiamide (Omniscan; GE Healthcare, Waukesha, Wis) per kilogram of body weight at 4 mL/sec, followed by injection of 20 mL saline at 4 mL/sec, with an electronic power injector (Spectris Solaris; Medrad, Indianola, Pa). This sequence combines TREAT with parallel imaging, as previously described (17). The k-space segmentation factor was three. Patients were instructed to hold their breath in full inspiration, and image acquisition was started simultaneously with contrast material injection.
Conventional single-phase MR angiography.—After a 2-mL timing bolus was injected to determine the contrast material arrival time, single-phase high-spatial-resolution 3D contrast-enhanced MR angiography of the thorax was performed by using a gradient-recalled echo sequence before (mask data set) and after injection of 0.15 mmol/kg gadodiamide (2.87/0.97; flip angle, 30°; bandwidth, 610 Hz/pixel; field of view, 406 x 500 mm2; matrix, 358 x 512; voxel size, 1.4 x 1.0 x 1.6 mm3; number of partitions, 72; generalized autocalibrating partially parallel acquisition factor, two; acquisition time, 19 seconds). Two postcontrast data sets were acquired in each patient. The contrast material injection rate was 1.5 mL/sec. The contrast material bolus was followed by injection of 20 mL saline at 1.5 mL/sec. Imaging was started at the time of contrast material arrival in the pulmonary arteries, and patients were asked to hold their breath in full inspiration.
In all patients, both time-resolved and conventional MR angiography were successfully performed after uneventful administration of the contrast agent.
Postprocessing.—For time-resolved angiographic data sets, magnitude subtraction in the image domain of the first (unenhanced) data set from all subsequent data sets was performed online, as was on-axis maximum intensity projection (MIP) reconstruction. Therefore, the subtracted images, the unsubtracted images, and MIPs of each phase were available for immediate viewing. Magnitude subtraction of the mask images from the contrast-enhanced images was also performed for the single-phase high-spatial-resolution data sets. Both the subtracted and the unsubtracted images were available for subsequent image analysis, as were full-thickness MIP sets and overlapping thin MIP reconstructions in multiple planes.
MR Angiographic Image Analysis
All MR images were independently evaluated by two imagers with experience in imaging patients with CHD (H.D., with 5 years of experience, and M.H.L., with 10 years of experience). The image series of each patient were evaluated in a random order. The observers were blinded to the results of other diagnostic examinations but were aware of the main diagnosis and major surgical procedures in each patient. Both the time-resolved MR angiographic series and the conventional MR angiographic series were evaluated qualitatively for image quality and the presence of artifacts. Image quality was rated by using a four-point scale, with a score of 0 indicating poor (nondiagnostic) image quality; a score of 1, fair image quality, with reservations about diagnostic content; a score of 2, good image quality, with confidence in diagnostic content; and a score of 3, excellent image quality, with very high confidence in diagnostic content. Presence of artifacts was rated by using a four-point scale, with a score of 0 indicating no artifact; a score of 1, mild artifact, not interfering with diagnostic content; a score of 2, moderate artifact, degrading diagnostic content; and a score of 3, severe artifact, resulting in nondiagnostic images.
Lung perfusion was assessed in the time-resolved and conventional MR angiographic data sets by evaluating the degree of enhancement of the pulmonary parenchyma on a regional, relative basis. Each lung was divided into three segments (upper, middle, and lower), and perfusion was rated by using a four-point scale, with a score of 0 indicating absent perfusion; a score of 1, diminished perfusion; a score of 2, normal perfusion; and a score of 3, abnormally increased perfusion.
In the time-resolved MR angiographic series, the sequence in which structures, including postsurgical conduits and shunts, enhanced was recorded.
Each two-dimensional cardiac SSFP cine and velocity-encoded cine MR imaging data set was assessed for disease or dysfunction (eg, blood shunting, septal defect, defective valvular and myocardial function) by viewing the image series at a workstation; evident disease or dysfunction was recorded. The observers integrated the MR angiographic findings with the findings on multiplanar cardiac SSFP cine and velocity-encoded cine MR images.
After review of the time-resolved and conventional MR angiographic data sets, each observer summarized what additional clinical information, if any, was gained from time-resolved MR angiographic data. Furthermore, information that was evident at both MR angiography examinations, as well as disease or dysfunction that was missed at time-resolved angiography, was recorded by the observers.
Statistical Analysis
A Wilcoxon signed rank test was used to test for statistical differences between the image quality ratings of the two observers. Interobserver variability (
) for rating of pulmonary perfusion and blood shunting and assessment of surgical conduits was calculated.
All statistical tests were two tailed, and differences with P < .05 were regarded as statistically significant. The statistical tests were performed by using software (SPSS, version 11.0; SPSS, Chicago, Ill).
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RESULTS
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Image Quality and Artifacts
The time-resolved and conventional MR angiographic data sets, respectively, had mean image quality scores of 2.6 ± 0.5 (standard deviation) and 2.7 ± 0.5 for observer 1 and 2.8 ± 0.4 and 2.7 ± 0.5 for observer 2. No statistically significant difference was evident between the scoring of the two observers (P = .32 for time-resolved and P = .47 for conventional MR angiography). In terms of artifact grading, from among a total of 81 studies, observer 1 scored seven time-resolved (motion artifact, n = 4; respiration artifact, n = 4; aliasing, n = 1) and 14 high-spatial-resolution data sets (motion artifact, n = 6; respiration artifact, n = 9; aliasing, n = 1) as having mild artifacts and two time-resolved (stent and/or coil artifact, n = 2) and four high-spatial-resolution data sets (motion artifact, n = 1; respiration artifact, n = 2; stent and/or coil artifact, n = 2) as having moderate artifacts. Likewise, observer 2 rated four time-resolved (motion artifact, n = 2; respiration artifact, n = 1; stent artifact, n = 1) and 10 high-spatial-resolution data sets (motion artifact, n = 3; respiration artifact, n = 8; stent artifact, n = 1) as having mild artifacts and one time-resolved (stent and/or coil artifact) and one high-spatial-resolution data set (stent and/or coil artifact) as having moderate artifacts.
Pulmonary Perfusion Assessment
Concordant results for subjective interpretation of bilateral pulmonary perfusion on the time-resolved and high-spatial-resolution MR angiographic images were recorded for 53 and 67 of 81 patients by observers 1 and 2, respectively. Observer 1 reported higher confidence in the assessment of lung perfusion with the time-resolved study than with the high-spatial-resolution study in a total of 38 patients (observer 2: 30 patients). In studies with discordance between pulmonary perfusion as visualized with both techniques, observers 1 and 2 had more confidence in time-resolved than in conventional MR angiography for 22 and 10 patients, respectively.
CHD Assessment
Cine and flow imaging.—Cardiac cine imaging was most useful for the assessment of intracardiac morphology and cardiac function. Important information concerning global and regional cardiac function was evident in 11 and six patients, respectively. Additionally, valvular stenosis, valvular insufficiency, or other valvular disease was diagnosed in 22, 48, and 17 patients, respectively, by means of cine MR imaging. In 24 patients, enlargement of at least one cardiac chamber was observed on cine images, and myocardial hypertrophy was noted in 23 patients. ASDs or VSDs were visualized in 11 patients with right-to-left shunting noted in the time-resolved MR angiographic series (Fig 1). However, for four studies in which shunting was diagnosed in the time-resolved series, no morphologic septal defect was detected on the cine images.

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Figure 1a: Images in 26-year-old man with cyanosis secondary to total anomalous pulmonary venous return (type II, drainage into coronary sinus) and large ASD. (a) Six of 13 coronal images from time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) are shown as projection angiograms. Early enhancement of aorta (arrow in A and B) consistent with ASD and right-to-left blood shunting is observed. After enhancement of aorta, pulmonary arteries (arrows in C) appear enhanced. Contrast material arrival in pulmonary veins (vertical arrows in E), followed by a second enhancement of the aorta (horizontal arrow in E, arrow in F), is observed. (b) Coronal MIPs from high-spatial-resolution MR angiography (2.87/0.97; flip angle, 30°) in anterioposterior projection and with ±15° rotation. Branching of right and left carotid arteries from brachiocephalic artery (arrow), which can merely be suspected with the time-resolved image series, is clearly visualized. (c) Diastolic (left) and systolic (right) image frames from double-oblique four-chamber cine SSFP MR imaging sequence (2.4/1.2; flip angle, 65°) show the large ASD (white arrows). An enlarged right ventricle (*) with right ventricular myocardial hypertrophy (black arrows) can also be appreciated.
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Figure 1b: Images in 26-year-old man with cyanosis secondary to total anomalous pulmonary venous return (type II, drainage into coronary sinus) and large ASD. (a) Six of 13 coronal images from time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) are shown as projection angiograms. Early enhancement of aorta (arrow in A and B) consistent with ASD and right-to-left blood shunting is observed. After enhancement of aorta, pulmonary arteries (arrows in C) appear enhanced. Contrast material arrival in pulmonary veins (vertical arrows in E), followed by a second enhancement of the aorta (horizontal arrow in E, arrow in F), is observed. (b) Coronal MIPs from high-spatial-resolution MR angiography (2.87/0.97; flip angle, 30°) in anterioposterior projection and with ±15° rotation. Branching of right and left carotid arteries from brachiocephalic artery (arrow), which can merely be suspected with the time-resolved image series, is clearly visualized. (c) Diastolic (left) and systolic (right) image frames from double-oblique four-chamber cine SSFP MR imaging sequence (2.4/1.2; flip angle, 65°) show the large ASD (white arrows). An enlarged right ventricle (*) with right ventricular myocardial hypertrophy (black arrows) can also be appreciated.
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Figure 1c: Images in 26-year-old man with cyanosis secondary to total anomalous pulmonary venous return (type II, drainage into coronary sinus) and large ASD. (a) Six of 13 coronal images from time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) are shown as projection angiograms. Early enhancement of aorta (arrow in A and B) consistent with ASD and right-to-left blood shunting is observed. After enhancement of aorta, pulmonary arteries (arrows in C) appear enhanced. Contrast material arrival in pulmonary veins (vertical arrows in E), followed by a second enhancement of the aorta (horizontal arrow in E, arrow in F), is observed. (b) Coronal MIPs from high-spatial-resolution MR angiography (2.87/0.97; flip angle, 30°) in anterioposterior projection and with ±15° rotation. Branching of right and left carotid arteries from brachiocephalic artery (arrow), which can merely be suspected with the time-resolved image series, is clearly visualized. (c) Diastolic (left) and systolic (right) image frames from double-oblique four-chamber cine SSFP MR imaging sequence (2.4/1.2; flip angle, 65°) show the large ASD (white arrows). An enlarged right ventricle (*) with right ventricular myocardial hypertrophy (black arrows) can also be appreciated.
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Flow quantification was performed in 35 of 81 patients for evaluation of the pulmonary valve and/or pulmonary arterial flow (n = 24), for evaluation of the aortic valve and/or flow in the ascending aorta (n = 6), for assessment of the peak flow and/or pressure gradient in cases of aortic coarctation (n = 7), and for measurement of blood flow in conduits (n = 3). Flow sequences revealed a pressure gradient over vascular stenoses by enabling measurement of the maximum blood flow velocity in 13 patients and were used to determine the regurgitation fraction in cases of valvular insufficiency in 14 patients. In five patients with aortic coarctation or recoarctation, the findings of time-resolved MR angiography and conventional MR angiography were supported by measurements of elevated peak velocities or pressure gradients across the coarctation site. In two patients who had previously undergone repair of aortic coarctation, a significant stenosis could be ruled out with MR angiography and flow measurements. Conventional MR angiography, time-resolved MR angiography, and flow measurements showed open conduits in three patients.
Time-resolved and single-phase MR angiography.—Observers 1 and 2 found important functional information (including that related to assessment of pulmonary perfusion) that was not seen at conventional MR angiography in the time-resolved MR angiographic series in 52 and 51 patients, respectively. Intra- and extracardiac shunts, respectively, were visualized exclusively with time-resolved angiography by observer 1 in 18 (observer 2: 15) and two (observer 2: two) patients, whereas a baffle leak or an intracardiac shunt was ruled out in 14 patients by both observers (Fig 2). Patency of Glenn or Fontan shunts was better visualized in the time-resolved MR angiography series in six patients by both observers, whereas occlusion of the left innominate vein was seen in one patient by both observers only at time-resolved MR angiography.

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Figure 2a: Images in 40-year-old woman with history of tricuspid atresia who had undergone left Blalock-Taussig shunt placement and Glenn and modified Fontan shunt placement and who had a residual VSD and "functional univentricle." (a) Five of 13 coronal images from time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) shown as projection angiograms depict open Glenn shunt to right pulmonary artery (arrow in B). Rapid transit of contrast material from right pulmonary artery to pulmonary veins (arrowhead) suggests intrapulmonary shunting. Left subclavian artery is occluded at its origin (arrow in C), consistent with a history of left Blalock-Taussig shunt placement. (b) Four coronal arterial phase high-spatial-resolution MR angiograms (2.87/0.97; flip angle, 30°) show various small collateral vessels (arrows in A) from thoracic aorta to right pulmonary artery. Prominent right upper pulmonary vein (arrowhead) draining into left atrium is also visible, as is occluded left subclavian artery (arrow in C). Although there is some enhancement of pulmonary arteries in left lung (arrow in D), the open modified Fontan shunt supplying the left lung could be appreciated only on late-phase MR angiograms (not shown).
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Figure 2b: Images in 40-year-old woman with history of tricuspid atresia who had undergone left Blalock-Taussig shunt placement and Glenn and modified Fontan shunt placement and who had a residual VSD and "functional univentricle." (a) Five of 13 coronal images from time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) shown as projection angiograms depict open Glenn shunt to right pulmonary artery (arrow in B). Rapid transit of contrast material from right pulmonary artery to pulmonary veins (arrowhead) suggests intrapulmonary shunting. Left subclavian artery is occluded at its origin (arrow in C), consistent with a history of left Blalock-Taussig shunt placement. (b) Four coronal arterial phase high-spatial-resolution MR angiograms (2.87/0.97; flip angle, 30°) show various small collateral vessels (arrows in A) from thoracic aorta to right pulmonary artery. Prominent right upper pulmonary vein (arrowhead) draining into left atrium is also visible, as is occluded left subclavian artery (arrow in C). Although there is some enhancement of pulmonary arteries in left lung (arrow in D), the open modified Fontan shunt supplying the left lung could be appreciated only on late-phase MR angiograms (not shown).
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Vascular diseases or disorders of large vessels—for example, aortic coarctation or morphology of right ventricular outflow tract and pulmonary artery—were well visualized with both MR angiographic techniques (Figs 3, 4).

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Figure 3a: Images in 42-year-old man with history of aortic coarctation that had been surgically repaired and in whom restenosis was suspected. (a) Five of 14 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly depict recoarctation (arrows), which is also evident (arrows) on (b) coronal volume-rendering technique images. Note that images in b are displayed in posteroanterior direction with different angulations. (c) Hemodynamic importance of recoarctation (arrow) is shown as irregular flow (arrowhead) on double-oblique SSFP cine MR images (2.4/1.2; flip angle, 65°). No substantial collateral vessels were seen with either imaging technique.
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Figure 3b: Images in 42-year-old man with history of aortic coarctation that had been surgically repaired and in whom restenosis was suspected. (a) Five of 14 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly depict recoarctation (arrows), which is also evident (arrows) on (b) coronal volume-rendering technique images. Note that images in b are displayed in posteroanterior direction with different angulations. (c) Hemodynamic importance of recoarctation (arrow) is shown as irregular flow (arrowhead) on double-oblique SSFP cine MR images (2.4/1.2; flip angle, 65°). No substantial collateral vessels were seen with either imaging technique.
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Figure 3c: Images in 42-year-old man with history of aortic coarctation that had been surgically repaired and in whom restenosis was suspected. (a) Five of 14 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly depict recoarctation (arrows), which is also evident (arrows) on (b) coronal volume-rendering technique images. Note that images in b are displayed in posteroanterior direction with different angulations. (c) Hemodynamic importance of recoarctation (arrow) is shown as irregular flow (arrowhead) on double-oblique SSFP cine MR images (2.4/1.2; flip angle, 65°). No substantial collateral vessels were seen with either imaging technique.
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Figure 4a: Images in 16-year-old female patient who had undergone kidney transplantation and was suspected of having abnormal infradiaphragmatic pulmonary venous return. (a) Six of 16 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly show partial abnormal pulmonary venous return involving right lower pulmonary vein draining into inferior vena cava (scimitar vein) (arrows). Homogeneous perfusion of transplanted kidney is also depicted (arrowheads). Coronal (b) thin MIPs and (c) volume-rendering technique image (in anteroposterior direction) also show the scimitar vein (white arrows), as well as normal enhancement of the arterial and venous vessels of the transplanted kidney (black arrow and arrowhead in b; arrowheads in c).
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Figure 4b: Images in 16-year-old female patient who had undergone kidney transplantation and was suspected of having abnormal infradiaphragmatic pulmonary venous return. (a) Six of 16 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly show partial abnormal pulmonary venous return involving right lower pulmonary vein draining into inferior vena cava (scimitar vein) (arrows). Homogeneous perfusion of transplanted kidney is also depicted (arrowheads). Coronal (b) thin MIPs and (c) volume-rendering technique image (in anteroposterior direction) also show the scimitar vein (white arrows), as well as normal enhancement of the arterial and venous vessels of the transplanted kidney (black arrow and arrowhead in b; arrowheads in c).
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Figure 4c: Images in 16-year-old female patient who had undergone kidney transplantation and was suspected of having abnormal infradiaphragmatic pulmonary venous return. (a) Six of 16 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) clearly show partial abnormal pulmonary venous return involving right lower pulmonary vein draining into inferior vena cava (scimitar vein) (arrows). Homogeneous perfusion of transplanted kidney is also depicted (arrowheads). Coronal (b) thin MIPs and (c) volume-rendering technique image (in anteroposterior direction) also show the scimitar vein (white arrows), as well as normal enhancement of the arterial and venous vessels of the transplanted kidney (black arrow and arrowhead in b; arrowheads in c).
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However, in 27 patients, vascular details that were not well shown at time-resolved MR angiography were seen at high-spatial-resolution MR angiography. Specifically, observer 1 had higher confidence in the assessment of the branching of supraaortic vessels in 12 patients (observer 2: 11 patients) (Fig 1), and, in eight patients (observer 2: 10 patients), major aortopulmonary collateral arteries were better visualized at conventional MR angiography (Fig 5). For both observers, accessory renal arteries were visualized in six patients only at conventional MR angiography, and coarctation of the aorta and open conduits (Fontan or Glenn), respectively, were seen exclusively at conventional MR angiography in one patient by observer 1 and two patients by observer 2 and in four patients by observer 1 and two patients by observer 2. Details of the visualization of most important morphologic and functional features at MR angiography are given in Table 3.

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Figure 5a: Images in 15-year-old male patient with D-transposition of great arteries and VSD who had undergone surgical bidirectional connection of superior vena cava and right pulmonary artery (Glenn shunt placement). (a) Six of 13 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) show early enhancement of right and left pulmonary arteries due to open Glenn shunt (horizontal arrows). Reduced perfusion of right upper lobe (arrowhead) that likely reflects perfusion via aortopulmonary collateral vessels is seen. Asymmetric temporal venous drainage, with early venous drainage of right inferior pulmonary vein (vertical arrow), followed by left inferior and left superior pulmonary veins, is observed. Right superior pulmonary vein shows delayed venous drainage. (b) Volume-rendering technique reconstructions of coronal high-spatial-resolution MR angiographic data (2.87/0.97; flip angle, 30°) in posteroanterior view. Widely patent Glenn shunt (arrow) is seen in left image, whereas in the right image, at least three prominent collateral vessels (arrows) originating from the proximal descending aorta and supplying the right upper lobe can be seen. Those collateral vessels were not directly visualized at time-resolved MR angiography. (c) Double-oblique SSFP cine MR image (2.4/1.2; flip angle, 65°) shows large ASD (black arrow) with left-to-right shunting and a high VSD (white arrow).
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Figure 5b: Images in 15-year-old male patient with D-transposition of great arteries and VSD who had undergone surgical bidirectional connection of superior vena cava and right pulmonary artery (Glenn shunt placement). (a) Six of 13 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) show early enhancement of right and left pulmonary arteries due to open Glenn shunt (horizontal arrows). Reduced perfusion of right upper lobe (arrowhead) that likely reflects perfusion via aortopulmonary collateral vessels is seen. Asymmetric temporal venous drainage, with early venous drainage of right inferior pulmonary vein (vertical arrow), followed by left inferior and left superior pulmonary veins, is observed. Right superior pulmonary vein shows delayed venous drainage. (b) Volume-rendering technique reconstructions of coronal high-spatial-resolution MR angiographic data (2.87/0.97; flip angle, 30°) in posteroanterior view. Widely patent Glenn shunt (arrow) is seen in left image, whereas in the right image, at least three prominent collateral vessels (arrows) originating from the proximal descending aorta and supplying the right upper lobe can be seen. Those collateral vessels were not directly visualized at time-resolved MR angiography. (c) Double-oblique SSFP cine MR image (2.4/1.2; flip angle, 65°) shows large ASD (black arrow) with left-to-right shunting and a high VSD (white arrow).
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Figure 5c: Images in 15-year-old male patient with D-transposition of great arteries and VSD who had undergone surgical bidirectional connection of superior vena cava and right pulmonary artery (Glenn shunt placement). (a) Six of 13 images from coronal time-resolved MR angiographic series (2.01/0.81; flip angle, 20°) show early enhancement of right and left pulmonary arteries due to open Glenn shunt (horizontal arrows). Reduced perfusion of right upper lobe (arrowhead) that likely reflects perfusion via aortopulmonary collateral vessels is seen. Asymmetric temporal venous drainage, with early venous drainage of right inferior pulmonary vein (vertical arrow), followed by left inferior and left superior pulmonary veins, is observed. Right superior pulmonary vein shows delayed venous drainage. (b) Volume-rendering technique reconstructions of coronal high-spatial-resolution MR angiographic data (2.87/0.97; flip angle, 30°) in posteroanterior view. Widely patent Glenn shunt (arrow) is seen in left image, whereas in the right image, at least three prominent collateral vessels (arrows) originating from the proximal descending aorta and supplying the right upper lobe can be seen. Those collateral vessels were not directly visualized at time-resolved MR angiography. (c) Double-oblique SSFP cine MR image (2.4/1.2; flip angle, 65°) shows large ASD (black arrow) with left-to-right shunting and a high VSD (white arrow).
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Interobserver Agreement
Interobserver agreement for greater confidence in the assessment of lung perfusion by using the time-resolved MR data sets was good (
= 0.65; 95% confidence interval: 0.48–0.82). Similarly, interobserver agreement for detection of blood shunting and assessment of surgical conduits or grafts was very good, yielding
values of 0.84 (95% confidence interval: 0.70–0.99) and 0.84 (95% confidence interval: 0.72–0.96), respectively.
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DISCUSSION
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The results of our study indicate that time-resolved 3D MR angiography has an important role to play in the evaluation of patients with juvenile and adult CHD. By defining visually the sequence of enhancement of the central blood vessels, lungs, and cardiac chambers, time-resolved MR angiography provides functional and anatomic information that complements or supplements that provided by conventional MR angiography and cardiac cine imaging. Furthermore, only a small additional dose of contrast medium is necessary.
Technical Considerations
Modern MR imaging unit technology allows the use of short repetition and echo times in combination with parallel imaging, making possible highly time-resolved angiographic 3D acquisitions with good spatial resolution (12). Previous studies involved the use of time-resolved angiography for the evaluation of peripheral arterial occlusive disease (14) or carotid artery disease (18), as well as for the assessment of intracranial vascular malformations (19). Several methods for temporally resolved MR angiography have been described. Time-resolved imaging of contrast kinetics, or TRICKS (20), is a technique for time-resolved 3D MR angiography whereby low-spatial-frequency data are sampled more often than are high-spatial-frequency data. The latter are shared among neighboring frames to generate a full k-space data set for each frame. In our study, a similar technique of temporal interpolation (ie, TREAT) was used to increase the apparent temporal resolution by approximately 30%. However, our method also incorporated parallel imaging (17), which further increased resolution by a factor of almost two. So that we could acquire one 3D data set within less than 1.5 seconds, spatial resolution in the partition-encoding direction was traded for time to produce rapid, quasiprojection angiograms. Therefore, when compared with conventional 3D MR angiography, time-resolved 3D MR angiography has limited through-plane resolution and lower in-plane resolution, and the MIPs cannot usefully be viewed off-axis. However, the inherent 3D nature of the projections can be appreciated by reviewing partitions or by viewing volume-rendered data sets. With conventional 3D MR angiography, although spatial resolution is greater, the complex nature of vessel overlap can be troublesome on MIPs, and it is usually necessary to review the partition MR images or multiplanar reformations (10,11).
Clinical Implications
It has been well established that cardiac cine MR imaging is accurate in the assessment of cardiac morphology and function. Valvular insufficiency and stenosis are depicted with high clinical accuracy (21,22). Furthermore, transvalvular flow measurements can be successfully performed and pressure gradients estimated in stenotic vessels (23). Time-resolved MR angiography provides a different perspective on functional vascular anatomy and pulmonary perfusion, complementing cardiac cine imaging and flow imaging on one hand and single-phase high-spatial-resolution MR angiography on the other. In our study, 11 patients with ASDs or VSDs at cine imaging had right-to-left shunting that was shown at time-resolved MR angiography. However, in another four patients with unequivocal shunting at time-resolved MR angiography, no morphologic correlate for the shunts could be visualized in available cine series. This may be due to "blind spots" or partial-volume effects in the assessment of the atrial or ventricular septum with two-dimensional cine sequences.
The reliability of the time-resolved MR angiographic data sets is underscored by the good interobserver agreement found for greater confidence in the assessment of lung perfusion, detection of blood shunting, and assessment of surgical conduits or grafts.
Results of previous studies (24) have indicated that time-resolved angiographic sequences are extremely efficient in terms of the amount of anatomic coverage per unit of imaging time compared with other sequences. In patients with CHD in whom echocardiography fails to depict extracardiac vascular anatomy, contrast-enhanced MR angiography can be applied successfully. Time-resolved MR angiography provides a rapid overview of the status and patency of vascular structures. With only small contrast material doses, time-resolved MR angiography may be utilized to detect intra- and extracardiac shunts, to measure circulation times, and to evaluate dynamic vascular anatomy in thoracic vascular disease (12).
In our study, Fontan and Glenn shunt patency was better appreciated in six patients by both observers at time-resolved MR angiography. The dynamic sequence of enhancement was frequently helpful in detecting the presence and/or patency of shunts or conduits. Also, the sequence of enhancement was rated by both observers to be absolutely essential for the evaluation of two patients with complex cardiac anatomy and complex postsurgical status. Furthermore, time-resolved MR angiography was especially useful in showing right-to-left shunting of blood (19 patients) and depicting altered pulmonary perfusion patterns. Pulmonary malperfusion is common in pre- and postsurgical patients with adult CHD (25,26) and may affect the long-term prognosis and follow-up strategy (27). Although pulmonary perfusion may also be derived from the appearance of the pulmonary arteries, normal and abnormal perfusion patterns are much more easily appreciated by using a dynamic image series. Although assessment of contrast material kinetics was not performed in our study, the high temporal resolution may also be used for the assessment of contrast material kinetics in different vascular territories to determine, for example, pulmonary transit time or capillary perfusion (28–30).
Five of the 81 patients in our study had undergone previous Senning or, Mustard surgical correction of a D-transposition of the great arteries. Besides mild baffle leaks, which are common and do not require treatment, a severe baffle leak is a rare but potentially serious complication in these patients that requires surgical reintervention (31,32) and may be assessed by using cine cardiac imaging. However, our study results show that with time-resolved MR angiography, a baffle leak could be confidently ruled out.
Even though, compared with single-phase MR angiography, only a fraction of the contrast material dose was used, time-resolved MR angiography revealed important morphologic information—for example, aortic coarctation and dilation or stenosis of the right ventricular outflow tract and/or pulmonary arteries. Similarly, venous disease or disorder (eg, stenosis or occlusion of the superior vena cava) was detected in six patients with both MR angiographic sequences. Although all abnormalities of the supracardiac veins were evident at time-resolved MR angiography owing to injection of the contrast material in an upper extremity vein, in some patients image acquisition was not sufficiently prolonged for enhancement of the inferior vena cava. Therefore, stenosis or occlusion of the inferior vena cava in two patients and patency of a Fontan shunt in another two patients were missed at time-resolved MR angiography but were evident at conventional MR angiography. This limitation can be addressed by extending the image acquisition period beyond the breath-holding interval, especially with evolving data processing capabilities.
Because of its higher spatial resolution relative to that of time-resolved MR angiography, finer vascular detail (as in aortopulmonary collateral vessels) was better appreciated at conventional MR angiography. Major aortopulmonary collateral arteries were diagnosed by observer 1 exclusively or with higher confidence in eight patients (observer 2: 10 patients) at conventional MR angiography. Anatomic variants or disease of the supraaortic vessels could not reliably be determined in 12 patients at time-resolved MR angiography.
Our study had limitations. Not all of the findings noted at time-resolved MR angiography were compared with findings of other imaging techniques. For example, results of lung scintigraphy were not routinely available for correlation with the dynamic MR imaging data. However, in many of the patients evaluated, particularly those with shunts, strict comparison of (static) lung scintigraphic findings with dynamic first-pass MR angiography would be difficult. Second, our study population is somewhat heterogeneous and comprised patients with a broad range of abnormalities and previous surgical procedures. Nonetheless, the CHD in our patients is representative of the spectrum of CHD now prevalent in the community, and, as we have shown, many different disease entities are excellent candidates for functional MR angiography. Finally, we did not perform quantification of lung perfusion, shunting, circulation times, and conduit or graft flows. Although these measurements could have been performed, interpretation of the results is not straightforward in all cases. Our study was therefore limited to a subjective evaluation of the dynamic time-resolved data.
In conclusion, compared with conventional MR angiography, time-resolved 3D MR angiography yields clinically relevant information in a substantial number of patients such that, where available, the techniques should be regarded as complementary.
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ADVANCES IN KNOWLEDGE
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- Important functional information that was not seen at high-spatial-resolution MR angiography was found in time-resolved MR angiography series in more than 60% (51 of 81) of our patients.
- By defining visually the sequence of enhancement of the central blood vessels, lungs, and cardiac chambers, time-resolved MR angiography provides functional and anatomic information that complements or supplements that of conventional MR angiography and cardiac cine imaging.
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IMPLICATIONS FOR PATIENT CARE
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- Time-resolved MR angiography can be effective in "unraveling" complex vascular anatomy and flow processes in patients with congenital heart disease (CHD).
- With only a small amount of contrast agent, time-resolved MR angiography can complement conventional MR angiography in the diagnosis and follow-up of patients with CHD.
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FOOTNOTES
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Abbreviations: ASD = atrial septal defect CHD = congenital heart disease MIP = maximum intensity projection SSFP = steady-state free precession 3D = three-dimensional TREAT = time-resolved echo-shared angiographic technique VSD = ventricular septal defect
See Materials and Methods for pertinent disclosures.
Author contributions: Guarantors of integrity of entire study, M.F., J.P.F.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, all authors; statistical analysis, M.F., K.N., S.G.R., J.C., J.P.F.; and manuscript editing, all authors.
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