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Breath-hold FLASH and FISP Cardiovascular MR Imaging: Left Ventricular Volume Differences and Reproducibility¹

¹ From the Cardiovascular Magnetic Resonance Unit, Royal Brompton Hospital, Sydney St, London SW3 6NP, England (J.C.C.M., C.H.L., J.M.F., G.C.S., D.J.P.); and Siemens Medical Solutions, Erlangen, Germany (C.H.L.). Received July 11, 2001; revision requested August 20; final revision received December 10; accepted December 20. Supported by CORDA and the Wellcome Trust. J.C.C.M. supported by the British Heart Foundation. Address correspondence to J.C.C.M. (e-mail: j.moon@rbh.nthames.nhs.uk).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
PURPOSE: To compare fast imaging with steady-state precession (FISP) and fast low-angle shot (FLASH) magnetic resonance acquisitions to quantify left ventricular volumes, mass, and function and to determine if the two techniques are comparable.

MATERIALS AND METHODS: Left ventricular volume studies were performed in 10 patients with heart failure and in 10 healthy subjects by using FISP and FLASH imaging. Identical section positions were used for section-by-section contour comparisons. Manual analysis was performed by two experienced observers. The study was repeated on a different day and interobserver and interstudy reproducibility assessed.

RESULTS: With FISP, end-diastolic volume was larger (healthy subjects: +18 mL [13%], P < .001; patients: +6 mL [3%], not significant), end-systolic volume larger (healthy subjects: +9 mL [17%], P = .001; patients: +8 mL [6%], P = .001) and left ventricular mass smaller (healthy subjects: -25 g (19%), P < .001; patients: -21 g (11%), P < .001). There were no significant differences in ejection fraction. Both sequences had excellent interstudy and interobserver reproducibility, with statistically better reproducibility for interstudy healthy-subject ejection fraction on FISP images (P = .05). Section-by-section analysis determined that at FISP, endocardial contours were drawn larger and the epicardial contours smaller than on FLASH images. FISP enabled better delineation of epicardial fat from myocardium, of blood-myocardium interface in areas of trabeculation or papillary muscles, and of the atrioventricular ring.

CONCLUSION: FISP produces small but significantly higher left ventricular volume measurements, as compared with FLASH imaging. FLASH imaging and FISP have similar reproducibility.

© RSNA, 2002

Index terms: Heart, MR, 51.12144, 51.121416 • Magnetic resonance (MR), motion studies, 51.12144

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Cine cardiovascular magnetic resonance (MR) imaging with conventional gradient-echo sequences (breath holding, segmented fast low-angle shot [FLASH], and other variants) is accurate and reproducible for the assessment of cardiac volumes, mass, and function (1–4). With the establishment of normal reference ranges (5–10), a single assessment can provide important diagnostic and prognostic information, while serial assessment benefits from the high reproducibility of the technique, allowing close monitoring of remodeling.

Recent advances in imager hardware have permitted the introduction of potentially improved cine sequences. These steady-state free precession sequences were designated as fast imaging with steady-state precession (FISP) and implemented as TrueFISP; as balanced fast-field echo imaging; or as fast imaging employing steady-state acquisition, or FIESTA, depending on the manufacturer (11). Such sequences rephase the transverse magnetization that undergoes dephasing during phase encoding and readout between radio-frequency pulses; therefore, imaging occurs when all transverse and longitudinal magnetization components are at steady state (12).

This results in substantially improved blood-myocardium contrast (13), being dependent mainly on the tissue to blood T₁/T₂ ratio and not on through-plane blood flow (14). This may allow easier delineation of the endocardial borders, particularly in areas affected by slow flow, such as around the papillary muscles. At the epicardial border, fat-myocardium delineation may also be improved, although there remains the potential for artifact from field inhomogeneities, susceptibility effects, and artifacts related to eddy current induction. These characteristics mean that cardiac volume, mass, and function analysis may differ between steady-state free precession and conventional gradient-echo sequences.

Therefore, the purpose of our study was to compare FISP and FLASH acquisitions for quantification of left ventricular (LV) volumes, mass, and function and to determine if the two techniques are comparable.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Study Population
Twenty subjects were included in the study: 10 (four men, six women; mean age, 32 years; range, 27–44 years) consecutive healthy adult volunteers with no known risk factors or history of cardiac disease and 10 patients (eight men, two women; mean age, 62 years; range, 19–84 years) who had previously undergone cardiovascular MR imaging and had chronic stable heart failure (New York Heart Association class I–III with ischemic, dilated, or valvular cardiomyopathy; mean ejection fraction, 44% ± 13). The patients were recruited from a dedicated heart failure clinic. For interstudy variability, examinations were repeated on different days 7–28 days later. Thus, each of 20 subjects underwent two pairs of complete volume studies, totaling 80 volume studies. The study was approved by the institutional ethics committee, and all subjects gave written informed consent.

Image Acquisition
Imaging was performed with a 1.5-T imager (Sonata; Siemens, Erlangen, Germany) by using front and back surface coils and prospective electrocardiographic triggering. The study was designed to test potential differences in analysis arising from the different sequence properties rather than from reproducibility of acquisition, so all imaging examinations were performed by the same operator (J.C.C.M.). Imaging consisted of acquisition of FISP scout images and subsequent two- and four-chamber cine images. Breath-hold short-axis sections were acquired from the atrioventricular ring to the apex, with a 7.0-mm section thickness and a 3.0-mm gap and one section per breath hold, according to our standard in-house clinical protocol.

Section positioning was identical for the FISP and FLASH sequences. All imaging was performed with breath holding at end expiration. The sequence parameters were selected for consistency in temporal and spatial resolution between FISP and FLASH sequences and were standard sequences in clinical use.

The number of cardiac phases per acquisition was 80%–90% of the R-R interval divided by the temporal resolution (FLASH, 56 msec; FISP, 48 msec), with eight to 12 sections to cover the LV. FLASH imaging parameters were an echo time of 6.1 msec, in-plane pixel size of 2.1 x 1.4 mm, section thickness of 7.0 mm, flip angle of 20°, and acquisition time of 15 heartbeats. FISP imaging parameters were a repetition time msec/echo time msec of 3.2/1.6, in-plane pixel size of 2.3 x 1.4 mm, section thickness of 7.0 mm, flip angle of 60°, and acquisition time of 12 heartbeats.

Image Analysis
Analysis was performed with a personal computer (model P600; Dell Computers UK, Bracknell, Berkshire, UK) by using in-house software (CMRtools; Imperial College, London, England). The FISP and FLASH volume series for each patient were separated and presented for analysis with blinding to patient details, although the acquisition technique could not be blinded because of distinct differences in appearance between image types. The end-systolic (ES) frames were chosen by the first observer (J.C.C.M.) and then used by both observers (C.H.L.). In this manner, systolic contours drawn on the same section by different observers could be compared as part of the section-by-section analysis. Furthermore, this ensured that differences in ES parameters were due to the image appearance and not to the selection of different images in the cardiac cycle. On each end-diastolic (ED) frame, endocardial and epicardial borders were manually traced, and only an endocardial border was traced on the ES frame. These areas were summed without rendering or smoothing to calculate ventricular volumes. Myocardial mass was determined by multiplying myocardial tissue volume by the specific gravity of 1.05. All contours drawn were saved for section-by-section comparison. Because border identification is partly subjective, a fixed set of criteria was used to determine borders to minimize interobserver and intraobserver variability, as described previously (5). These considerations included drawing contours with reference to the section above and below and after viewing the whole cine loop if necessary, including papillary muscles and trabeculations within the LV mass and excluding right ventricular trabeculations arising from the interventricular septum from the LV mass.

Reproducibility
To assess the reproducibility of the two techniques, interstudy variability was assessed for each technique. To ensure that any differences between techniques were observer independent, interobserver variability was assessed by having a second observer (C.H.L.) analyze the first FISP and FLASH volume studies in each subject. Thus, 120 volume analyses were performed in total.

Section-by-Section Analysis
After all contours were drawn, FISP and FLASH acquisitions for each subject were compared section by section from base to apex.

Differences in volumes and mass were assigned in each section in three categories: (a) Differences in endocardial contour (resulting in differences in mass and volume) between techniques, (b) differences in epicardial contour (resulting in differences in mass) between techniques, and (c) differences in selection of the basal or apical section.

In addition, by scaling the ventricles from "most basal" to "most apical" to compensate for different ventricular lengths, systematic differences in endocardial and/or epicardial contour tracing from base to apex were assessed for each technique.

When basal and apical sections were selected differently for the two techniques, independent qualitative review was performed by two observers (J.C.C.M., C.H.L.) to determine which technique appeared more accurate, with agreement in all cases, without the need for consensus.

Statistical Analysis
Differences between FISP and FLASH results for ED and ES volume, ejection fraction, and mass were assessed by using the paired Student t test. Power calculations to assess the minimum FISP-FLASH difference detectable in this study were not possible in advance because there was no estimate available of the SD of the FISP-FLASH difference. They were, however, subsequently performed on the FISP-FLASH results to calculate the minimum detectable difference (80% power, = .05) with the study. Interobserver and interstudy (test-retest) reproducibility for the preceding parameters were assessed by calculating the coefficient of variability (equal to the SD of the difference between two measurements over the mean of the two measurements, expressed as a percentage). The statistical significance of differences in reproducibility was assessed by using an extension of the method of Bland and Altman (15), as described in the Appendix.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Image and Contour Comparison
A typical volume acquisition for a healthy subject and patient is shown in Figure 1. A single section with the independently drawn contours overlaid and compared is shown in Figure 2. Differences in epicardial and endocardial contours between FISP and FLASH images were evident; the endocardial contours differed most around papillary muscles and trabeculations, and the entire epicardial contour appeared smaller on FISP images, as compared with FLASH images.

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. (a) Sample short-axis stack volume acquisitions at ED in a healthy subject. Top panel is FLASH acquisition, the lower, FISP. The superior image quality of FISP is evident. Imaging parameters for FLASH imaging were echo time, 6.1 msec; pixel size, 2.1 x 1.4 x 7.0 mm; flip angle, 20°; and 15-heartbeat acquisition time. FISP parameters were 3.2/1.6; pixel size, 2.3 x 1.4 x 7.0 mm; flip angle, 60°; and acquisition time, 12 heartbeats (b) Sample short-axis stack volume acquisitions at ED in a patient. Images presented in same order as for a.

View larger version (139K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. (a) Sample short-axis stack volume acquisitions at ED in a healthy subject. Top panel is FLASH acquisition, the lower, FISP. The superior image quality of FISP is evident. Imaging parameters for FLASH imaging were echo time, 6.1 msec; pixel size, 2.1 x 1.4 x 7.0 mm; flip angle, 20°; and 15-heartbeat acquisition time. FISP parameters were 3.2/1.6; pixel size, 2.3 x 1.4 x 7.0 mm; flip angle, 60°; and acquisition time, 12 heartbeats (b) Sample short-axis stack volume acquisitions at ED in a patient. Images presented in same order as for a.

View larger version (131K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Single short-axis section obtained in a healthy subject (upper left quadrant) and a patient (lower left quadrant). Left panel shows the raw image, middle panel shows the epicardial and endocardial contours (drawn independently), and right panel shows the overlaid FISP and FLASH imaging contours. Short arrows indicate areas where the FISP endocardial contour increases ED volume, reducing LV mass. Long arrow indicates example of FLASH imaging epicardial contour, including epicardial fat in the LV mass. Imaging parameters for FLASH imaging were echo time, 6.1; pixel size, 2.1 x 1.4 x 7.0 mm; flip angle, 20°; and acquisition time, 15 heartbeats. FISP parameters were 3.2/1.6; pixel size, 2.3 x 1.4 x 7.0 mm; flip angle, 60°; and acquisition time, 12 heartbeats.

View larger version (21K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Graphs show differences in (a) healthy subjects and (b) patients for section-by-section comparison of the area enclosed by the FISP contour minus that enclosed by FLASH from base to apex. LV mass is smaller at FISP in all locations from base to apex. In healthy subjects, this arises from the larger FISP endocardial area; in patients it arises from a larger FISP endocardial area and a smaller FISP epicardial contour. Dashed line = diastolic epicardial area, thin solid line = diastolic endocardial area, dotted line = systolic endocardial area, thick solid line = myocardial area.

View larger version (21K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Graphs show differences in (a) healthy subjects and (b) patients for section-by-section comparison of the area enclosed by the FISP contour minus that enclosed by FLASH from base to apex. LV mass is smaller at FISP in all locations from base to apex. In healthy subjects, this arises from the larger FISP endocardial area; in patients it arises from a larger FISP endocardial area and a smaller FISP epicardial contour. Dashed line = diastolic epicardial area, thin solid line = diastolic endocardial area, dotted line = systolic endocardial area, thick solid line = myocardial area.

Basal and apical section selection.— Despite identical section positioning, an extra basal ED section was selected for the FLASH volume study, as compared with the FISP study, in four of 20 analyses in the healthy subjects and in two of 20 analyses in the patients. Piloting had been designed to accurately position the basal section across the atrioventricular valve plane for both types of acquisition, and comparison with the FISP study showed the extra section selection to be incorrect. Likewise, occasional discrepancies occurred at the apex, although these had far lesser effects on the analysis. These sections were excluded from comparative analysis. The dominant contribution of these different effects to differences in results was the larger endocardial contours for both volume and mass analysis. Qualitative review where differences occurred showed definition of the fibrous atrioventricular ring to be better with FISP, appearing darker than myocardium. It was not clear which technique resulted in better definition at the apex.

Reproducibility
The interobserver and interstudy reproducibility of FISP and FLASH imaging are shown in Figure 4. Of the 16 reproducibility comparisons, only interstudy ejection fraction reproducibility in healthy subjects was statistically significant, favoring FISP. Therefore, FISP has similar reproducibility to FLASH imaging.

View larger version (23K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Graphs show interobserver (A, C) and interstudy (B, D) reproducibility of FISP (white bars) versus FLASH (black bars) imaging quantified by the coefficients of variability in the healthy subjects (A, B) and patients (C, D). EDV = ED volume, ESV = ES volume. In B, * = P = .05; this is the only significant result.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

Therefore, there is a question as to which measurement technique is more accurate. The best technique for resolving differences or bias between two indirect measurement techniques is to calibrate them, either against a known quantity or against a highly accurate direct method. Phantom studies could be used; however, FISP-FLASH differences are likely to be flow related, occurring either at complicated blood-myocardium interfaces or at fat-myocardium boundaries. Differentiating these complex issues would require complicated phantoms and substantial extrapolation to the in vivo situation. Calibration of MR imaging has been previously performed in animal models or human cadavers (4,5,16–24). These studies mostly involve comparison of actual LV weight with cardiovascular MR imaging–derived mass (Table 2). Overview of these studies suggests a trend toward overestimation of LV mass with cardiovascular MR imaging, where 47 hearts (animal and human) in five studies suggest overestimation, whereas two studies in 18 hearts suggest underestimation, with the remainder showing no bias. In the two studies of human cadaver hearts (20,23), overestimation of true mass with cardiovascular MR imaging averaged 4.8%. However, sequence design and hardware advances have permitted a progression from free-breathing spin-echo imaging to breath-hold cine imaging and mean that there are considerable differences in the techniques used in many of these studies, as compared with current techniques. In addition, the canine model has limitations because there are species-specific differences in epicardial fat distribution and LV trabeculation. Canine epicardial fat is dependent on breed, nutrition, and exercise regimen, and the LV is less trabeculated than in humans (25). FLASH and FISP sequences could be calibrated against explanted human hearts, but in practice these studies are difficult to perform and the time between imaging and transplantation unpredictable and often long, and it cannot be assumed that the heart remains the same during this interval. Thus, in neither canine nor human studies are ventricular volumes likely to be calibrated to the accuracy required.

From the data presented here, these volumetric differences arise for two reasons: The endocardial contour was drawn larger and the epicardial contour drawn smaller in FISP. For the endocardial contour, the surface slow-flow boundary layer around papillary muscles and trabeculations on FLASH images can make papillary muscles appear larger and confluent with the myocardium and can make blood between trabeculations appear as myocardium. An equivalent effect can be found if LV mass is assessed in systole, when trabeculae are more confluent (28). The importance of trabeculae and papillary muscles for LV parameters has been previously commented on (29). Further expansion of the perceived blood pool and reduction in LV mass may arise, since voxels containing both blood and myocardium may be perceived as myocardial at FLASH imaging but as blood pool at FISP because of the relatively higher blood signal at FISP. Both effects can be observed in Figures 1 and 2. For the epicardial contour, epicardial fat can be difficult to distinguish from myocardium at FLASH imaging, particularly in patients in whom there may be some motion artifact, but is more readily discerned at FISP. However, particularly in thin subjects, the myocardium-lung border can be more difficult to discern at FISP. There were some differences in basal section selection, but definition of the fibrous atrioventricular ring appeared better with FISP and darker than myocardium, suggesting that basal section selection is improved with FISP. The apex had a lesser contribution to LV measurement, since the volumes were small and it was less clear which technique was more accurate at the apex. These differences are summarized in Table 3.

The introduction of techniques with different reference ranges is not new. It is known that different noninvasive techniques (echocardiography, radionuclide ventriculography, angiography, and cardiovascular MR imaging) have different measurement properties and as a consequence have different reference ranges (30). With the continued evolution of cardiovascular MR imaging and the introduction of FISP and subsequent real-time techniques (31), automated contouring programs, and basal section tracking techniques (32), it will be important to ensure comparability between new and old techniques. If they are not comparable, it may be necessary to derive new reference ranges for each technique and to be aware of the differences when comparing images obtained with different techniques.

	APPENDIX

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Each study participant underwent two observations with each measurement technique. For each participant and technique, the squared difference between the two observations was an estimate of within-subject variance for that method multiplied by two. A paired t test can then be used to compare tests 1 and 2 squared differences if they are normally distributed, but this assumption was not met in this case. Therefore, natural log transformation of the squared differences was performed. If the squared difference was zero, it was replaced by half of the next smallest value before log transformation. A two-tailed paired t test can then be performed on the logged squared differences for the two tests. Further details of this statistical technique can be found on the Web site of J. Martin Bland, PhD: www.sghms.ac.uk/depts/phs/staff/jmb /jmb.htm.

	ACKNOWLEDGMENTS

 
We thank J. Martin Bland, PhD, of the Department of Public Health Sciences, St George’s Hospital Medical School, London, England, for statistical advice.

	FOOTNOTES

 
Abbreviations: ED = end diastole, ES = end systole, FISP = fast imaging with steady-state precession, FLASH = fast low-angle shot, LV = left ventricular

Author contributions: Guarantor of integrity of entire study, D.J.P.; study concepts and design, J.C.C.M., C.H.L., D.J.P.; literature research, J.C.C.M., C.H.L., D.J.P.; clinical studies, J.C.C.M., C.H.L., J.M.F., G.C.S.; data acquisition, J.C.C.M., C.H.L., G.C.S.; data analysis/interpretation, J.C.C.M., C.H.L., D.J.P.; statistical analysis, J.C.C.M., C.H.L., D.J.P.; manuscript preparation, all authors; manuscript definition of intellectual content, J.C.C.M., C.H.L., D.J.P.; manuscript editing, revision/review, and final version approval, all authors.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 

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