Comparison of native high-resolution 3D and contrast-enhanced MR angiography for assessing the thoracic aorta

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1 European Heart Journal Cardiovascular Imaging (2014) 15, doi: /ehjci/jet263 Comparison of native high-resolution 3D and contrast-enhanced MR angiography for assessing the thoracic aorta Florian von Knobelsdorff-Brenkenhoff 1 *, Henriette Gruettner 1, Ralf F. Trauzeddel 1, Andreas Greiser 2, and Jeanette Schulz-Menger 1 1 Working Group on Cardiovascular Magnetic Resonance, Experimental and Clinical Research Center, a Joint Cooperation Between the Charité Medical Faculty and the Max-Delbrueck Center for Molecular Medicine, and HELIOS Klinikum Berlin Buch, Department of Cardiology and Nephrology, Schwanebecker Chaussee 50, Berlin 13125, Germany; and 2 Siemens AG, Healthcare Sector, Erlangen, Germany Received 23 September 2013; revised 4 November 2013; accepted after revision 26 November 2013; online publish-ahead-of-print 7 January 2014 Aims To omit risks of contrast agent administration, native magnetic resonance angiography (MRA) is desired for assessing the thoracic aorta. The aim was to evaluate a native steady-state free precession (SSFP) three-dimensional (3D) MRA in comparison with contrast-enhanced MRA as the gold standard.... Methods Seventy-six prospective patients with known or suspicion of thoracic aortic disease underwent MRA at 1.5 T using (i) and results native 3D SSFP MRA with ECG and navigator gating and high isotropic spatial resolution ( mm 3 ) and (ii) conventional contrast-enhanced ECG-gated gradient-echo 3D MRA ( mm 3 ). Datasets were compared at nine aortic levels regarding image quality (score 0 3: 0 ¼ poor, 3 ¼ excellent) and aortic diameters, as well as observer dependency and final diagnosis. Statistical tests included paired t-test, correlation analysis, and Bland Altman analysis. Native 3D MRA was acquired successfully in 70 of 76 subjects (mean acquisition time min), while irregular breathing excluded 6 of 76 subjects. Aortic diameters agreed close between both methods at all aortic levels (r ¼ 0.99; bias + SD mm) with low intra- and inter-observer dependency (intraclass correlation coefficient 0.99). Native MRA studies resulted in the same final diagnosis as the contrast-enhanced MRA. The mean image quality score was superior with native compared with contrast-enhanced MRA ( vs ; P, 0.001).... Conclusion Accuracy of aortic size measurements, certainty in defining the diagnosis and benefits in image quality at the aortic root, underscore the use of the tested high-resolution native 3D SSFP MRA as an appropriate alternative to contrast-enhanced MRA to assess the thoracic aorta Keywords Aorta Magnetic resonance Angiography Native Introduction Detailed, accurate, and robust imaging of the thoracic aorta is crucial to reliably detect aortic diseases and exactly monitor their course in order to make appropriate clinical decisions. Magnetic resonance angiography (MRA) with blood enhancement by an intravenously administered, gadolinium-containing, T 1 -shortening contrast agent is regarded as one of the gold standard for this purpose. 1 Despite the proven evidence regarding its accuracy and clinical value, contrast-enhanced MRA has some drawbacks: MR contrast agents have to be carefully considered in patients with severe renal dysfunction due to the risk of nephrogenic systemic fibrosis 2 and sometimes cause acute reactions. 3 They are expensive and require venous access at costs of time, material, and the risk of extravasation of contrast agent in the surrounding soft tissue. 4 Exact timing to achieve maximum intraluminal contrast can be a challenge, and image acquisition requires breath holding, which not all patients tolerate appropriately. Finally, if given for MRA, the contrast media cannot be given during the same session for other cardiovascular applications like stress perfusion. 5 Native steady-state free precession (SSFP) angiography is one potential alternative to overcome most of these limitations. Previous * Corresponding author. Tel: ; Fax: , florian.von-knobelsdorff@charite.de Published on behalf of the European Society of Cardiology. All rights reserved. & The Author For permissions please journals.permissions@oup.com

2 652 F. von Knobelsdorff-Brenkenhoff et al. studies already reported satisfactory agreement between native aortic imaging and contrast-enhanced MRA as the gold standard. 6 9 In the present study, we introduce an optimized three-dimensional (3D) protocol with high spatial resolution and isotropic voxel dimension, and test it in a large cohort for the assessment of the thoracic aorta in comparison with ECG-gated contrast-enhanced MRA. Methods Patients Patients were eligible to enter the study if they were sent for standard MRA with a clinical indication. Between 2010 and 2012, 76 patients were prospectively enrolled into the study and underwent cardiovascular MR (CMR). The patients characteristics and indications for CMR are described in Table 1. The local ethics committee approved the study, and all participants provided informed consent. Image acquisition All examinations were performed by specialized technicians and supervised by experienced physicians (SCMR Level 3) using a 1.5-T MR system (Magnetom Avanto, Siemens AG, Healthcare Sector, Erlangen, Germany). A six-element body matrix and a six-element spine matrix coil were used for signal reception and the body coil for transmission. The CMR protocol started with localizers, followed by the native thoracic angiography and a standard contrast-enhanced MRA of the thoracic aorta. Depending on the clinical question, SSFP cine imaging for cardiac chamber quantification, or valvular assessment, phase-contrast flow measurements or late-enhancement imaging were added. Table 1 Patients characteristics and indications for CMR (mean + standard deviation) Parameter Result... N 76 Sex (males/females) 50/26 Age (years) Height (cm) Weight (kg) Body surface area (m 2 ) Heart rate (1/min) Left ventricular end-diastolic volume (ml) Left ventricular end-diastolic volume index (ml/cm) Left ventricular mass (g) Left ventricular mass (g/cm) Left ventricular ejection fraction (%) Main indication for MRA Suspicion/control of ascending aortic aneurysm 56 Suspicion of aortic dissection 1 Suspicion/control of aortic coarctation 4 Comprehensive evaluation of aortic valve disease 7 Follow-up after aortic surgery (ductus Botalli closure, 5 Ross procedure, replacement of ascending aorta) Suspicion of coronary artery aneurysm 1 Miscellaneous 2 (i) Native 3D MRA: the sequence applied was a 3D, segmented SSFP sequence with non-selective radiofrequency (RF) excitation. The field of view (FOV) was selected to cover the whole chest to avoid wrap-around due to the non-slice-selective RF excitation. Data acquisition was performed in coronal orientation with a right-to-left phase-encoding direction. To minimize cardiac motion artefacts, prospective ECG gating with data acquisition during diastole was applied (acquisition period: 286 ms per cardiac cycle). T 2 preparation (echo time, TE: 40 ms) was done in each heartbeat to increase the blood pool-tissue contrast. To reduce breathing motion artefacts, a respiratory navigator-gated technique with two intersecting slices on the liver and prospective slice following was used (respiratory gating window +4 mm). After the navigator pulses, a frequencyselective fat-saturation pulse was applied to suppress the fat signal, followed by a non-selective RF excitation during the SSFP preparation and data acquisition. At the end of the data acquisition, a gradient spoiler was used to avoid spillover of the protons transverse magnetization into the next R R interval. 8 Imaging parameters were: FOV mm 2, matrix size , slice thickness 1.3 mm (no interpolation), leading to a true voxel size of mm 3, flip angle (FA) 908, bandwidth 967 Hz/pixel, TE 1.1 ms, repetition time (TR) 2.3 ms, 60 segments, parallel imaging (GRAPPA) with acceleration factor 2, and 24 integrated reference lines. (ii) Contrast-enhanced 3D MRA: A 3D FLASH pulse sequence with prospective ECG gating was used for contrast-enhanced 3D MRA. An acquisition period was 486 ms per cardiac cycle and covered both systole and early diastole. The imaging slab was defined in an oblique sagittal orientation to cover the complete thoracic aorta. An unenhanced mask was acquired for the final subtraction to eliminate background signals. A test bolus of contrast agent (amount: 2 ml, flow rate: 2 ml/s, Gadoteridol, Bracco, Italy), followed by a saline flush (20 ml, 2 ml/s), was given using an automatic infusion pump (Medrad, Bayer, Germany) to define the optimal acquisition time. The MRA was obtained after intravenous administration of 0.2 mmol/kg body weight contrast media (minus the 2 ml test bolus) with a flow rate of 2 ml/s (saline flush 20 ml, 2 ml/s). Imaging parameters were: FOV mm 2, matrix , slice thickness 1.8 mm, voxel size mm 3, bandwidth 650 Hz/pixel, TE 1.1 ms, TR 2.7 ms, FA 258, parallel imaging (GRAPPA) with acceleration factor 2, and 24 integrated reference lines. 7 Image interpretation All images were read using the software CMR 42 (Circle Cardiovascular Imaging, Calgary, Canada). Multiplanar reconstructions of the thoracic aorta were used. The thoracic aorta was evaluated qualitatively and quantitatively at predefined levels adopted from the current guidelines: 1,10 (1) aortic annulus; (2) sinus of Valsalva; (3) sinotubular junction; (4) mid-ascending aorta (at the level of the pulmonary artery bifurcation); (5) proximal aortic arch (at the level of the right brachiocephalic trunk); (6) middle aortic arch (between the common carotid artery and the left subclavian artery); (7) proximal descending aorta (2 cm distal of the left subclavian artery); (8) middle descending aorta (middle between the left subclavian artery and the diaphragm); and (9) diaphragm (hiatus) (2 cm proximal of the coeliac trunk) (Figure 1). Qualitatively: first, the overall image quality was scored as 0 ¼ poor, non-diagnostic, 1 ¼ impaired image quality that may lead to misdiagnosis; 2 ¼ good; and 3 ¼ excellent, for each aortic level. The decision was based on border sharpness and image contrast. Secondly, the final diagnosis was noted. Thirdly, the visibility of both coronary ostia was rated as yes or

3 Comparison of different MR angiography assessing the thoracic aorta 653 Figure 1 Aortic levels for the evaluation of image quality and the quantification of aortic diameters. The images stem from a native 3D MRA. In the centre is a longitudinal view of the thoracic aorta. The surrounding pictures show the corresponding cross-sections at nine aortic levels: (1) aortic annulus; (2) sinus of Valsalva; (3) sinotubular junction; (4) mid-ascending aorta (at the level of the pulmonary artery bifurcation); (5) proximal aortic arch (at the level of the right brachiocephalic trunk); (6) middle aortic arch (between the common carotid artery and the left subclavian artery); (7) proximal descending aorta (2 cm distal of the left subclavian artery); (8) middle descending aorta (middle between the left subclavian artery and the diaphragm); and (9) diaphragm (hiatus) (2 cm proximal of the coeliac trunk). 10 no as a marker of aortic root sharpness. Quantitatively, the aortic diameter was measured on each aortic level. Thereby, the mean of the anterior posterior and left right diameter was calculated. Measurement was done from inner edge to inner edge. 10 To assess observer variability, one investigator read 45 randomly selected studies twice with a time latency of at least 3 months, and a second reader, who was blinded to the other reader s results, analysed 25 of those, too. The observer analysis included the evaluation of image quality and the quantification of the aortic diameters. Statistical analysis Quantitative measurements of aortic dimensions were compared by the paired t-test after testing for normality with the Kolmogorov Smirnov test, the Pearson correlation, and Bland Altman analysis. Qualitative assessments were compared using the Wilcoxon test. Observer dependency was tested using Bland Altman analysis and intraclass correlation coefficient. A P-value of,0.05 was regarded as statistically significant. Statistical analysis was performed using SPSS 20.0 (IBM, Armonk, NY, USA), and results presented using Prism 5.0 (GraphPad Software, San Diego, CA, USA). Results Feasibility Contrast-enhanced 3D MRA was performed successfully in all 76 subjects, and native 3D MRA in 70 of 76 subjects. The mean image acquisition time of the native 3D MRA was (range 3 16) min. Figure 2 provides a sample of examples obtained with both techniques. Acquisition was technically infeasible in 6 of 76 subjects (7.9%), with inefficient navigator due to irregular breathing. The final sample to compare aortic dimensions and image quality consisted of 70 subjects. Due to suboptimal positioning of the FOV, the diaphragm could not be evaluated in one case of native 3D MRA, as well as the middle aortic arch and the proximal descending aorta each in one case of native and contrast-enhanced MRA. Aortic dimensions Of 630 aortic segments, a total of 618 segments were eligible for aortic size measurements using the contrast-enhanced MRA and 623 using native MRA. The diameter of the aortic annulus could

4 654 F. von Knobelsdorff-Brenkenhoff et al. Figure 2 Set of examples of the native MRA (left) and the contrast-enhanced MRA (right): (A) Thoracic aorta with normal dimensions. The sharpness of the aortic root achieved with the native MRA (left) is visible in comparison with the blurry borders provided by the contrast-enhanced MRA (asterisk; right). (B) Large ascending aortic aneurysm. (C) Aortic coarctation (white arrow). Again, the blurry aortic root with the contrast-enhanced MRA is recognizable (asterisk; right). (D) Ascending aorta in a patient with previous mechanical aortic valve replacement. Note that the left main coronary artery is visible on the native MRA. (E) A large aneurysm of one sinus of Valsalva (black arrow). The regurgitant jet of the aortic valve is visible on the native MRA as it is acquired in diastole (white arrow). (F) Plaque in the descending aorta (white arrow). (G) State after surgical correction of a patent ductus arteriosus (white arrow). (H ) The proximal parts of the right and left coronary artery are visible on the native MRA, while they are not detectable on the contrast-enhanced MRA. (I) This patient has a coronary aneurysm due to Kawasaki syndrome with previous stent implantation during acute coronary syndrome. Both the aneurysm and the stent can be better delineated with the native MRA compared with the contrast-enhanced MRA. not be quantified due to impaired image quality in 10 of 70 subjects (14.3%) on contrast-enhanced MRA and in 4 of 70 subjects (5.7%) on native MRA. Figure 3 illustrates the correlation (r ¼ 0.99) and the Bland Altman plot (mean difference + SD mm) for all aortic measurements. The averaged diameter and the analysis of agreement between both methods for each aortic level are summarized in Table 2. There was no significant difference between both methods at 6 of 9 aortic levels (aortic annulus, sinus of Valsalva, mid-ascending aorta, proximal aortic arch, proximal descending aorta, and diaphragm). At the sinotubular junction and middle descending aorta, contrast-enhanced MRA resulted in larger values than the native MRA (mean difference and mm, respectively). At the middle aortic arch, contrast-enhanced MRA resulted in smaller values than the native MRA (mean difference mm). There was no relationship between the aortic dimensions and the discrepancies between both methods (r ¼ 20.09, Figure 3). The intra- and inter-observer agreement for the quantification of aortic diameters was satisfactory for both methods (Table 3). Aortic findings All successfully acquired native MRA studies came up with the same diagnosis as the contrast-enhanced MRA as the gold standard. Considering the 76 contrast-enhanced MRA as the reference method, 19 studies were diagnosed as normal (mainly exclusion

5 Comparison of different MR angiography assessing the thoracic aorta 655 Figure 3 Comparison of all single measurements of the aortic diameters using the native MRA and the contrast-enhanced MRA. Left: Pearson correlation. Right: Bland Altman analysis. Table 2 Aortic diameter assessment with the native MRA vs. contrast-enhanced MRA Aortic level Native MRA Contrast-enhanced Difference P-value (mean + SD MRA (mean + SD (mean + SD in mm) in mm) in mm)... Annulus Sinus Sinotubular junction Mid-ascending aorta Proximal aortic arch Middle aortic arch Proximal descending aorta Middle descending aorta Diaphragm The difference refers to the Bland Altman analysis; the P-value refers to the paired t-test. SD, standard deviation. Table 3 Intra- and inter-observer variability for assessing image quality and aortic diameters Native MRA Contrast-enhanced... MRA... Mean + SD ICC Mean + SD ICC... Image quality Intra-observer Inter-observer Aortic diameter Intra-observer Inter-observer SD, standard deviation; ICC, intraclass correlation coefficient. of a suspected aortic aneurysm). Forty-nine were diagnosed with a dilated ascending aorta, one with a dilated sinus of Valsalva, and seven with aortic coarctation. Concomitantly, four exhibited aortic plaques (Figure 2). Under consideration of the 6 of 76 failing native MRA studies, which remained without final diagnosis, the sensitivity of the native MRA to find the correct diagnosis was 92.1%. Image quality A total of 627 aortic segments were scored regarding image quality on native 3D MRA images and 628 on contrast-enhanced 3D MRA. Across all aortic levels, the mean score was better for native MRA compared with contrast-enhanced MRA ( vs ; P, 0.001). For each aortic level, the frequency of image scores and the mean score are summarized in Figure 4 and Table 4, respectively. Native MRA exhibited a significantly higher score than contrast-enhanced MRA at all aortic levels. Reason for poor or impaired image quality of the contrast-enhanced studies was predominantly blurring due to motion (Figure 2). As a marker of aortic root sharpness, both coronary ostia could be detected in 61 of 70 (85.7%) of the native studies vs. 24 of 70 (34.3%) of the contrast-enhanced studies. The overall intra- and inter-observer agreement for the assigned quality grades was good for the contrast-enhanced and the native technique (Table 3).

6 656 F. von Knobelsdorff-Brenkenhoff et al. Figure 4 Frequency of image scores for each aortic level using the native MRA (top) and the contrast-enhanced MRA (bottom). The image quality was scored as 0 ¼ poor, non-diagnostic, 1 ¼ impaired image quality that may lead to misdiagnosis; 2 ¼ good; and 3 ¼ excellent. Discussion Thoracic aortic diseases are often missed because they are commonly asymptomatic or not properly registered using conventional imaging like echocardiography. 7 On the other hand, efficient surveillance of known aortic diseases using ionizing radiation or contrast-enhanced MR is under debate. 11,12 A non-invasive diagnostic tool free of ionizing radiation or contrast media might improve screening and monitoring of aortic diseases. The present study presents a native 3D SSFP MRA that achieved very good image quality, led to accurate aortic size measurements, and resulted in the correct final diagnosis in a large patient sample. The acquisition of the native MRA was robust, and the mean expenditure of time was reasonable. Both aspects are important for clinical acceptance. In subjects with poor navigator efficiency (in this study 8%, which is in the range of other reports 13 ), the use of an abdominal belt may further speed up image collection and reduce the number of dropouts. 13 In addition, technical improvements of the navigator technique are needed to reduce the number of dropouts. Novel hardware and software developments including new acceleration techniques already promise to decrease the scan time in the future. 14,15 Native MRA exhibited significantly better image quality than contrast-enhanced MRA particularly at the aortic root. This important observation is mainly attributable to the following aspect: both native MRA and contrast-enhanced MRA were acquired ECG-gated, as ECG gating has been demonstrated to improve the image quality especially at the aortic root by minimizing motion blurring. 16 Moreover, the image acquisition of the contrast-enhanced MRA has to fit within one breath-hold and has to be complete after the first pass of the contrast agent, while the native MRA is collected over many heartbeats and independent from the pass of contrast media. This allows for the native MRA to reduce the acquisition time per cardiac cycle to a minimum and to shift the acquisition into end-diastole, which finally leads to the absence of cardiac motion artefacts. In contrast, the contrast-enhanced MRA with its longer acquisition time per cardiac cycle is forced to extent the image acquisition to both the systolic and diastolic phase. This leads to motion artefacts of the contrast-enhanced MRA especially at the aortic root, where the systolic movement is most prominent, which

7 Comparison of different MR angiography assessing the thoracic aorta 657 Table 4 Image quality assessment of native MRA vs. contrast-enhanced MRA Aortic level Native MRA (mean + SD) Contrast-enhanced MRA (mean + SD) P-value... Annulus ,0.001 Sinus ,0.001 Sinotubular junction ,0.001 Mid-ascending aorta ,0.001 Proximal aortic arch ,0.001 Middle aortic arch ,0.001 Proximal descending aorta ,0.001 Middle descending aorta ,0.001 Diaphragm ,0.001 The image quality wasscored as 0 ¼ poor, non-diagnostic, 1 ¼ impaired image quality that maylead to misdiagnosis; 2 ¼ good; and 3 ¼ excellent. The P-value refersto the Wilcoxon test. SD, standard deviation. impacts both image quality and aortic size measurements. Previous studies have already demonstrated superiority of the native navigator approach compared with the breath-hold contrast-enhanced MRA, even though they were smaller in size and some of them compared towards non-ecg-gated contrast-enhanced MRA. 8,9,17 Francois et al. 9 reported a mean image quality score of the aortic root of 4.7 for 3D SSFP (1 ¼ non-diagnostic and 5 ¼ excellent) and of 3.8 for ECG-gated contrast-enhanced MRA in 23 subjects. Krishnam et al. 8 studied 50 subjects and found significantly higher visibility scores for the aortic root on native SSFP MRA compared with non-ecg-gated contrast-enhanced MR. Hence, the present study confirms the benefit of less motion blurring for the tested high-resolution native MRA in a large patient sample compared with ECG-gated contrast-enhanced MRA. Another factor that possibly promoted the better image quality scores for the native MRA is the visibility of the complete anatomy, including aortic lumen, wall, and surrounding tissue, which facilitates topographic orientation and enables better delineation of the aortic borders. Aortic diameters and the observer dependency for measuring aortic diameters agreed closely between the native and contrastenhanced MRA. Even though statistically, the diameters differed significantly on the sinotubular, middle aortic arch, and middle descending level, the absolute differences were very small, within the sub-millimetre range. This result is clinically important, as the management of aortic aneurysm mainly depends on the absolute aortic size and also annual extension rate. The current guidelines recommend with Class I that asymptomatic patients with thoracic aneurysm should be evaluated for surgical repair if the ascending aorta or aortic sinus diameter is 5.5 cm, or in the case of Marfan or other genetically mediated disorders even at smaller diameters ( cm depending on the condition). Furthermore, patients with a growth rate of.0.5 cm/year should be considered for surgery. 1 These recommendations underline that accurate measurements of the aortic diameter in the mm-range with the low observer and inter-study variability are mandatory for optimal patient management. The present study proves in a large sample that the native MRA is as accurate and observer-independent as the contrast-enhanced MRA, which is the current gold standard. Regarding the inter-scan variability of the native MRA, we assume a high robustness due to the standardized approach that only requires one rectangular FOV covering the whole chest, even though this aspect has not been tested explicitly in this study. Despite the general close agreement of aortic diameters between both methods, the Bland Altman analysis (Figure 3) also illustrated that, in some individuals, deviations of several millimetres occurred between both methods. This seems mainly attributable to differences in the selected plane. For example, the level of the pulmonary artery is not only a single slice position, but rather comprises a region. In the case of an aortic aneurysm, differences in the slice selection of few millimetres may result in differences in the aortic diameter of several millimetres. Making the correct diagnosis is decisive to manage the patient appropriately and to omit unnecessary further testing. If we exclude those subjects where the native MRA could not be obtained properly, we observed a complete agreement between native MRA and contrast-enhanced MRA regarding the final diagnosis. This result is in agreement with previous studies using native MRA. 8 Admittedly, the present study does not cover the complete spectrum of aortic diseases. Hence, further trials are needed to test its overall diagnostic accuracy. Apart from the strength to image the thoracic aorta, which was the main focus of this study, the native MRA depicts the anatomy of the whole thorax, whereas the contrast-enhanced MRA only shows the aortic lumen. Even though the benefit of this added information was not explicitly studied in the present series, the detailed overview of the thoracic anatomy appears useful in many clinical circumstances, like in congenital heart disease. 18 In conclusion, the native 3D SSFP MRAwith high isotropic resolution for imaging the thoracic aorta was successfully acquired in the majority of patients within a reasonable expenditure of time, led to a significant improvement of image quality particularly at the aortic root compared with the ECG-gated contrast-enhanced gold standard, and demonstrated close agreement to the contrast-enhanced 3D MRA regarding aortic dimensions and final diagnosis. These data underscore its use as an alternative to the conventional contrast-enhanced protocol. Despite that, technical improvements improving the performance of the navigator technique to control respiratory motion are needed.

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