Retrospective electrocardiogram (ECG)-gated cine

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1 Circ J 2017; 81: doi: /circj.CJ ORIGINAL ARTICLE Imaging Assessment of Left Ventricular Function and Mass on Free-Breathing Compressed Sensing Real-Time Cine Imaging Tomoyuki Kido, MD, PhD; Teruhito Kido, MD, PhD; Masashi Nakamura, MD, PhD; Kouki Watanabe, MD, PhD; Michaela Schmidt, PhD; Christoph Forman, PhD; Teruhito Mochizuki, MD, PhD Background: Compressed sensing (CS) cine magnetic resonance imaging (MRI) has the advantage of being inherently insensitive to respiratory motion. This study compared the accuracy of free-breathing (FB) CS and breath-hold (BH) standard cine MRI for left ventricular (LV) volume assessment. Methods and Results: Sixty-three patients underwent cine MRI with both techniques. Both types of images were acquired in stacks of 8 short-axis slices (temporal/spatial resolution, 41 ms/ mm 3 ) and compared for ejection fraction, end-diastolic and systolic volumes, stroke volume, and LV mass. Both BH standard and FB CS cine MRI provided acceptable image quality for LV volumetric analysis (score 3) in all patients (4.7±0.5 and 3.7±0.5, respectively; P<0.0001) and had good agreement on LV functional assessment. LV mass, however, was slightly underestimated on FB CS cine MRI (median, IQR: BH standard, 83.8 ml, ml; FB CS, 79.0 ml, ml; P=0.0006). The total acquisition times for BH standard and FB CS cine MRI were 113±7 s and 24±4 s, respectively (P<0.0001). Conclusions: Despite underestimation of LV mass, FB CS cine MRI is a clinically useful alternative to BH standard cine MRI in patients with impaired BH capacity. Key Words: Cardiac magnetic resonance imaging; Cardiac volume; Left ventricular function; Magnetic resonance imaging Retrospective electrocardiogram (ECG)-gated cine magnetic resonance imaging (MRI) with breath hold (BH) is generally considered the standard method for assessment of left ventricular (LV) function. 1,2 This imaging sequence, however, requires multiple BH scans to cover the entire LV, thus prolonging the duration of cardiovascular MRI (CMR). In addition, many patients who undergo CMR have dyspnea, and difficulty tolerating BH. Poor BH technique can lead to poor image quality and low accuracy of LV functional assessment. Several acceleration techniques have been developed to reduce the BH duration in cine MRI. 3 5 Recently, compressed sensing (CS) with sparse sampling and iterative reconstruction was proven to reduce MRI acquisition time drastically. 6 Clinical studies have reported the utility of this technique in cine MRI for assessment of LV function with 1.5-T and 3.0-T MRI scanners Prospective ECG-triggered CS cine MRI, however, might be unable to capture the first and last phases of the cardiac cycle, because the acquisition window is set to a fixed length at the beginning of the scan This often leads to underestimation of end-dia- stolic volume (EDV) and, consequently, variations in stroke volume (SV) and ejection fraction (EF) relative to ECG-gated retrospective standard cine MRI. 10 To overcome this limitation, imaging data have been acquired over 2 heart beats, thus capturing the complete end-diastole between the first and second heart beats. 10 Given that CS cine MRI has the advantage of being inherently insensitive to respiratory motion because of single-shot acquisition, 11,12 it is suitable for free-breathing (FB) imaging. The purpose of this study was therefore to compare the accuracy of FB full cardiac cycle CS and BH standard cine MRI at 3.0 T for LV volume assessment in patients with cardiac conditions. Methods Subjects This prospective study was approved by the ethics review board of Saiseikai Matsuyama Hospital. All participants gave written consent for participation in the study. Seventy-one consecutive patients who were scheduled to Received February 7, 2017; revised manuscript received April 11, 2017; accepted April 18, 2017; released online May 18, 2017 Time for primary review: 20 days Department of Radiology, Ehime University Graduate School of Medicine, Toon (Tomoyuki K., Teruhito K., M.N., T.M.); Department of Cardiology, Saiseikai Matsuyama Hospital, Matsuyama (K.W.), Japan; and Siemens Healthcare, Erlangen (M.S., C.F.), Germany Mailing address: Tomoyuki Kido, MD, PhD, Department of Radiology, Ehime University Graduate School of Medicine, 454 Shitsukawa, Toon , Japan. tomozo0421@gmail.com ISSN All rights are reserved to the Japanese Circulation Society. For permissions, please cj@j-circ.or.jp

2 1464 KIDO T et al. Table 1. Patient Characteristics Characteristics Patients (n=63) Sex (F/M) 17/46 Age (years) 71.1±9.0 Height (cm) 160.6±9.4 Weight (kg) 61.9±12.8 Body mass index (kg/m 2 ) 23.8±3.4 Heart rate (beats/min) 62.0±10.2 Clinical diagnosis Coronary artery disease 42 (67) Cardiomyopathy 13 (21) Valve disease 3 (5) Other 5 (8) Data given as mean ± SD or n (%). Statistical Analysis On the basis of distribution, continuous data are expressed as mean ± SD or median (IQR), as appropriate. Paired t-test was used to compare scan times between the 2 methods. Comparison of image quality, EDV, ESV, SV, EF, and LVED mass between BH standard and FB CS cine MRI was done using Wilcoxon matched-pair signed-rank test. Linear regression and Bland-Altman analyses were performed to assess the correlation and agreement between these LV measurements and to evaluate inter- and intraobserver variabilities in CS cine MRI. P<0.05 was considundergo CMR for various cardiac conditions were enrolled. All participants underwent cine MRI with BH standard and FB CS sequences. Patients with arrhythmia (n=5) or severely impaired BH capacity (n=3) were excluded. Finally, 63 patients were included for analysis of image quality and LV volume. Table 1 lists the subject characteristics. Data Acquisition All CMR was acquired with a clinical 3.0-T MRI scanner (MAGNETOM Skyra, Siemens Healthcare, Erlangen, Germany) with 48 receivers and 2 parallel transmit channels. Scout images were acquired to plan the cardiac axial views. Short-axis BH standard cine images were acquired in stacks of 8 contiguous slices with adequate slice gaps to cover the entire LV, using a segmented balanced steadystate free-precession sequence. Standard cine MRI was acquired during BH after inspiration, and this served as the reference standard. Immediately after BH standard cine MRI, FB CS real-time cine MRI was acquired using a prototype sequence with sparse incoherent sampling of k-space and non-linear iterative SENSE-type image reconstruction. Details regarding data acquisition and reconstruction of CS real-time cine MRI have been given in a previous report. 10 In the present study, temporal and spatial resolution as well as slice orientation were kept identical between the 2 cine MRI protocols. Imaging parameters are summarized in Table 2. Image Analysis Both types of cine images were visually assessed for image quality, with focus on the adequacy of contour detection for LV volumetry, and scored on a 5-point scale: 1, nondiagnostic; 2, poor; 3, adequate; 4, good; and 5, excellent (Figure 1). Images with score 3 were considered acceptable for LV volume analysis. For measurement of LV volume, stacks of 8 contiguous short-axis cine MR images were assessed independently by 2 radiologists with 7 and 5 years of experience in cardiac MRI. A dedicated software package (SYNAPSE VINCENT; Fujifilm, Tokyo, Japan) was used for quantitative assessment of EDV, end-systolic volume (ESV), SV, EF, and LV end-diastolic (LVED) mass in both cine MRI datasets. Epicardial and endocardial contours rendered by automated analysis were reviewed and manually corrected, if necessary. 10 Papillary muscles and trabeculations of the LV were included in the LV chamber volume. 13,14 Table 2. Imaging Parameters BH standard MRI FB CS MRI Sequence type 2-D cine true FISP 2-D cine true FISP ECG mode Retrospective gating Prospective triggering Repetition time (ms) Echo time (ms) FOV (mm) Image matrix Reconstructed spatial resolution (mm) Temporal resolution (ms) Slice thickness (mm) 6 6 No. slices 8 8 Slice gap (mm) Flip angle ( ) Bandwidth (Hz/pixel) 1, Cardiac phases No. BH 4 0 Acceleration factor No. iterations 80 BH, breath-hold; CS, compressed sensing; ECG, electrocardiogram; FB, free-breathing; FISP, fast imaging with steady-state free precession; FOV, field of view; MRI, magnetic resonance imaging.

3 Compressed Sensing Cine Imaging Under Free Breath 1465 ered statistically significant. All statistical analysis was performed using commercially available software (JMP version 11; SAS Institute, Cary, NC, USA). Sample size was calculated on the basis of the primary outcome of difference in EF between the 2 cine MRI methods. On sample size calculation analysis, 51 participants were required in order to obtain an absolute difference >6% in EF, with 80% power and a 2-sided significance level of 0.05, assuming a common SD of 15% for mean EF. This EF margin was considered as being within the clinically acceptable range on the basis of previous findings Results All 63 patients successfully underwent BH standard and FB CS cine MRI. The total acquisition time for standard BH and for FB CS cine MRI was 113±7 s (range, s; including recovery time between BH of 12 s), and 24±4 s (range, s), respectively (P<0.0001). The image quality score of FB CS cine MRI (3.7±0.5) was worse than that of BH standard cine MRI (4.7±0.5; P<0.0001). FB CS cine MRI for all patients, however, had acceptable image quality (score 3) for LV volume analysis. Interobserver agreement on image quality for BH standard (kappa score, 0.73) and FB CS (kappa score, 0.72) cine MRI was good for both. Representative sets of standard BH and FB CS cine MRI of a patient with suspected myocardial ischemia are shown in Figure 2. BH standard cine MRI was used as the standard reference for LV volumetry. Comparison of EDV, ESV, SV, LVED mass, and EF between the 2 imaging methods is given in Table 3. There were no significant differences in EDV, ESV, SV, or EF between BH standard and FB CS cine MRI. Relative to BH standard cine MRI, however, a small but significant underestimation of LVED mass was noted on FB CS cine MRI. Nevertheless, there was good agreement between the 2 methods for all measurements on linear regression analysis (Figure 3). On Bland-Altman analysis, the mean differences in LV measurements between BH standard and FB CS cine MRI were as follows: EDV, 2.1 ml (95% CI: 32.6 to 36.7 ml); ESV, 2.2 ml (95% CI: 18.8 to 23.2 ml); SV, 0.2 ml (95% CI: 23.6 to 23.3 ml); LVED mass, 4.3 g (95% CI: 22.5 to 13.9 g); and EF, 1.1% (95% CI: 11.9 to 9.6%; Figure 4). The interobserver ( 4.4 to 3.8%) and intraobserver ( 7.9 to 4.6%) variabilities for FB CS cine MRI measurements were excellent, with slopes of regression ranging from 0.88 to 1.02 and from 0.91 to 0.97, respectively (Table 4). Discussion Our previous study demonstrated that single BH CS realtime cine MRI could evaluate LV volume with excellent accuracy using acquisition of CS cine MRI data over 2 heart beats. 10 Given, however, that many patients who undergo CMR have dyspnea or shortness of breath, image acquisition over 2 heart beats increases the required BH time as well as patient burden. FB MRI could be an alternative approach in patients who cannot hold their breath adequately. In this study, we evaluated the accuracy of FB full cardiac cycle CS cine MRI in LV volumetry. FB CS cine MRI LV volumetry was in good agreement with that of BH standard cine MRI. There were no significant differences in EDV, ESV, SV, or EF between the 2 methods. This suggests that it is possible to capture the complete Figure 1. Image quality score: representative cine images. (A) Score 1; (B) score 2; (C) score 3; (D) score 4; and (E) score 5. Figure 2. Representative (A,C) breath-hold (BH) standard and (B,D) free-breathing (FB) compressed sensing (CS) cine magnetic resonance imaging (MRI) of a 66-year-old female patient with suspected myocardial ischemia. (A,B) End-diastolic and (C,D) end-systolic short-axis MRI of the left ventricle. Both observers rated (A,C) BH standard CS cine MRI quality as excellent (i.e., score, 5) and (B,D) FB CS cine MRI quality as good (i.e., score, 4).

4 1466 KIDO T et al. Table 3. LV Volumetry BH standard (n=63) FB CS (n=63) P value EDV (ml) ( ) ( ) 0.37 ESV (ml) 45.3 ( ) 48.2 ( ) 0.11 SV (ml) 73.1 ( ) 70.1 ( ) 0.92 LVED mass (g) 83.8 ( ) 79.0 ( ) * EF (%) 62.2 ( ) 61.2 ( ) 0.11 Data given as median (IQR). *P<0.05. EDV, end-diastolic volume; EF, ejection fraction; ESV, end-systolic volume; LV, left ventricular; LVED, left ventricular end-diastole; SV, stroke volume. Other abbreviations as in Table 2. Figure 3. Correlation between BH standard and FB CS cine magnetic resonance imaging (MRI) for parameters in the measurement of left ventricular (LV) volume: (A) end-diastolic volume (EDV); (B) end-systolic volume (ESV); (C) stroke volume (SV); (D) LV end-diastole (LVED) mass; and (E) ejection fraction (EF). Abbreviations as in Figure 2. end-diastole between the first and second heart beats by acquiring data over 2 heart beats and to successfully trace endocardial contours on CS cine MRI even during FB. In comparison with standard cine MRI, standard real-time cine MRI usually has reduced spatial and temporal resolution, which might lead to inaccuracy in the evaluation of cardiac function with highly accelerated cine MRI. 20 In this study, we achieved identical temporal and spatial resolution in both the reference standard technique and realtime cine MRI using the CS technique, which was reflected in the good agreement for LV volumetry between the 2 techniques. With regard to differences in LV volumetry between the 2 techniques, the 95% CI for all LV volume measurements obtained with FB CS cine MRI were wider compared with BH CS cine MRI in our previous study. 10 These differences might be explained by the difference in breathing during imaging. Given that BH standard cine MRI was acquired at inspiration, the effect of negative intrathoracic pressure on LV volume 21 and the slight differences in short-axis slice orientation between BH and FB MRI 22 might have had some effect on this result. The blurry image due to FB might also slightly impair the accuracy of the determination of endocardial contour. The differences, however, between BH standard and FB CS cine MRI were within the acceptable range for LV volumetry. Relative to standard BH cine MRI, we observed a significant underestimation of LVED mass in FB CS cine MRI. For measurement of LVED mass, both endocardial and epicardial contours are defined at end-diastole. In the present study, there were no significant differences in EDV between the 2 methods. This therefore suggests that the underestimation of LVED mass on FB CS cine MRI might have been mainly caused by inaccuracy in the definition of epicardial contours. One of the reasons for this inaccuracy might be the lower contrast between the myocardium and outer surrounding structures, such as the lungs or liver, in comparison with the contrast between the myocardium and LV cavity in balanced steady-state free precession cine MRI. Furthermore, the high sub-sampling feature of CS might lead to reduced definition of borders, which would make accurate delineation of the epicardial border even more challenging. The combination of these effects might have led to the significant underestimation of LVED mass on FB CS cine MRI in the present study. In comparison with BH standard cine MRI, FB CS cine MRI drastically reduced the total acquisition time. Although BH standard cine MRI is a well-established

5 Compressed Sensing Cine Imaging Under Free Breath 1467 Figure 4. Mean differences in left ventricle (LV) measurement between breath-hold standard and free-breathing compressed sensing cine magnetic resonance imaging: (A) EDV; (B) ESV; (C) SV; (D) LVED mass; and (E) EF. ( ) Mean difference; (- - -) 95% CI of the mean difference; ( ) 95% limits of agreement (i.e., mean ±1.96 SD). Abbreviations as in Figure 3. Table 4. Variability of FB CS Cine MRI Measurement Difference Variability (%) R 2 Slope P value Intraobserver variability EDV (ml) 0.8± ± <0.001 ESV (ml) 2.9± ± <0.001 SV (ml) 2.0± ± <0.001 LVED mass (g) 2.4± ± <0.001 EF (%) 1.7± ± <0.001 Interobserver variability EDV (ml) 0.4± ± <0.001 ESV (ml) 3.4± ± <0.001 SV (ml) 3.0± ± <0.001 LVED mass (g) 6.9± ± <0.001 EF (%) 2.3± ± <0.001 Data given as mean ± SD. Abbreviations as in Tables 2,3. technique with proven clinical reliability, rapid FB CS cine MRI is more time efficient and beneficial for patients with difficulty in holding breath. In this study, we excluded patients with arrhythmia or severely impaired BH capacity (8/71 enrolled patients; 11%) because the reference sequence used for LV volume analysis relies on regular heart beat and adequate BH. Standard cine MRI of such patients has been reported to often exhibit severe artefacts, which makes LV volume analysis challenging. 23,24 CS real-time cine MRI is a useful approach in such patients because single-shot acquisition is inherently insensitive to motion artefacts caused by arrhythmia or breathing. 11,12 We believe that the CS tech- nique can improve the adaptability of CMR and help promote its widespread clinical use. There are some limitations to this study. First, FB CS cine MRI was reconstructed using the MR scanner central processing unit at the end of data acquisition. The reconstruction time for all short-axis slices was approximately 3 min. Shorter reconstruction times, however, are desirable for achieving real-time visualization. We expect that more efficient CS reconstruction techniques with graphic processing unit-based reconstruction algorithms 25 can reduce the reconstruction time and overcome this limitation. Second, although the differences between the measurements of BH standard and FB CS cine MRI were within

6 1468 KIDO T et al. the acceptable range, there were relatively wide 95% limits of agreement in EDV and EF measurements. In this study, we used identical 8-slice short-axis cine MRI, performed as routine examination. The slice number is smaller than that in the previous report by Sudarski et al. 7 When a smaller number of cine slice images is used to evaluate LV volume, the difference in determination of the lowest slice has a larger effect on the variability of measurement. Hence, in the present study this small slice number affected the accuracy of the determination of the lowest slice, and increased the difference in EDV and EF. We expect that the variability in the measurement can be reduced by increasing the slice number. Finally, given that regional myocardial wall motion was not assessed in the present study, further evaluation is required to determine the accuracy of FB CS cine MRI for assessment of regional myocardial wall motion abnormalities. 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