JOURNAL OF MAGNETIC RESONANCE IMAGING 29:1293–1299 (2009)
Original Research
Whole Heart Magnetization-Prepared Steady-State Free Precession Coronary Vein MRI Christian T. Stoeck, MSc,1,2 Yuchi Han, MD,1 Dana C. Peters, PhD,1 Peng Hu, PhD,1 Susan B. Yeon, MD,1 Kraig V. Kissinger, BS, RT,1 Beth Goddu, RT,1 Lois Goepfert, RN, MS,1 Warren J. Manning, MD,1,3 Sebastian Kozerke, PhD,2 and Reza Nezafat, PhD1* Purpose: To compare two coronary vein imaging techniques using whole-heart balanced steady-state free precession (SSFP) and a targeted double-oblique spoiled gradient-echo (GRE) sequences in combination with magnetization transfer (MT) preparation sequence for tissue contrast improvement. Materials and Methods: Nine healthy subjects were imaged with the proposed technique. The results are compared with optimized targeted MT prepared GRE acquisitions. Both quantitative and qualitative analyses were performed to evaluate each imaging method. Results: Whole-heart images were successfully acquired with no visible image artifact in the vicinity of the coronary veins. The anatomical features and visual grading of both techniques were comparable. However, the targeted small slab acquisition of the left ventricular lateral wall was superior to whole-heart acquisition for visualization of relevant information for cardiac resynchronization therapy (CRT) lead implantation. Conclusion: We demonstrated the feasibility of wholeheart coronary vein MRI using a 3D MT-SSFP imaging sequence. A targeted acquisition along the lateral left ventricular wall is preferred for visualization of branches commonly used in CRT lead implantation. Key Words: 3D SSFP whole-heart MRI; coronary vein imaging; magnetization transfer contrast J. Magn. Reson. Imaging 2009;29:1293–1299. © 2009 Wiley-Liss, Inc.
1 Department of Medicine (Cardiovascular Division), Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts. 2 Institute for Biomedical Engineering, University and ETH Zurich, Switzerland. 3 Department of Radiology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts. Contract grant sponsor: the American Heart Association; Contract grant number: AHA SDG0730339N. *Address reprint requests to: Reza Nezafat, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, MA, 02215. E-mail:
[email protected] Received October 23, 2008; Accepted March 9, 2009. DOI 10.1002/jmri.21788 Published online in Wiley InterScience (www.interscience.wiley.com).
© 2009 Wiley-Liss, Inc.
CONGESTIVE HEART FAILURE (CHF) with impaired left ventricular (LV) systolic function is a common clinical syndrome representing the end-stage of several different cardiac diseases. Cardiac resynchronization therapy (CRT) is an effective adjuvant to pharmacological treatment in selected patients with systolic heart failure (1). For this therapy, transvenous LV lead implantation is performed to position a pacing lead in the lateral branch of the coronary vein system, located in the lateral wall of the LV. Optimum procedural planning and lead delivery requires knowledge of coronary vein anatomy before and during the lead implantation procedure. Additionally, knowledge of coronary vein anatomy in relation to the tissue characteristics of the underlying myocardium in the pacing sites could improve the efficacy of this therapy, thereby improving on the 30 – 40% nonresponder rate (1,2). It has been shown recently that CRT does not reduce LV dyssynchrony in patients with transmural scar tissue in posterolateral LV segments, resulting in clinical nonresponse to CRT (3). Recent studies have demonstrated the ability of cardiovascular MR (CMR) to image the coronary veins (4,5). An electrocardiogram (ECG) -triggered, three-dimensional (3D) targeted small slab (3– 4 cm) imaging sequence with respiratory navigator was previously proposed to image the coronary veins. Magnetization transfer (MT) contrast and spectrally selective fat saturation sequences were used to improve blood-myocardium contrast. Both spoiled gradient-echo (GRE) and steady-state free precession (SSFP) imaging sequences can be used in coronary vein imaging, but SSFP is less favorable at high spatial resolution due to prolonged repetition times (TRs). The spectral response of balanced SSFP shows signal loss at certain frequency intervals, which is referred to as “dark banding” (6). The frequency offset for banding artifacts is inversely proportional to TR of the SSFP imaging sequence. This will cause signal loss at or around the coronary vein (7), especially at higher spatial resolution, which has been previously used in double-oblique targeted acquisition where a longer TR shifts the frequency offset of the
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banding artifacts closer to the water resonance frequency. An alternative to a targeted acquisition is the wholeheart coronary vein imaging method. In this approach, a large 3D axial slab (⬃10 –12 cm) is prescribed to image the entire heart in a single acquisition. Several studies have demonstrated the advantages and disadvantages of each of these approaches in coronary artery imaging (8 –11). In coronary vein imaging, 3D visualization of the whole-heart acquisition is preferred for easier demonstration of the anatomical features for electrophysiologists who are generally not experienced with interpreting 3D small-slab targeted acquisition, where 3D volume rendering cannot be easily achieved. The wholeheart coronary vein imaging approach was recently demonstrated using an inversion recovery sequence with an exogenous intravascular (blood pool) gadolinium-based contrast agent and a T2 magnetization prepared whole-heart SSFP (5). Intravascular gadolinium contrast agents are not currently available for clinical use in the United States. In addition, few data are available on their use for delayed gadolinium enhancement scar imaging as this technique has been studied almost exclusively with extracellular rather than intravascular agents. A T2 magnetization prepared SSFP whole-heart imaging sequence yields significant signal loss in coronary veins (4,5). Therefore, an alternative noncontrast method is appealing for whole-heart coronary vein imaging. Use of a noncontrast coronary vein imaging method facilitates incorporation of a late gadoliniumenhanced viability scan using an extracellular contrast agent in the same imaging session. Although both GRE and SSFP can be used in targeted coronary acquisitions, SSFP has been the commonly used imaging sequence in whole-heart approaches due to its superior blood myocardium contrast-to-noise ratio (CNR) (8). Furthermore, SSFP sequences show an inherent MT contrast enhancement, as shown by (12,13) which might be beneficial for coronary vein imaging. In a thin slab acquisition, the inflow of fresh blood increases the blood signal-to-noise ratio (SNR) and yields better CNR for GRE imaging. Theoretically, the voxel SNR in whole-heart acquisitions is increased as a function of phase encodings in the third dimension. However, this improved SNR cannot be directly translated into an improved CNR. The higher slab thickness in a whole-heart versus targeted acquisition results in greater blood saturation from repeated radiofrequency (RF) excitation and a decrease in blood myocardium CNR. This RF saturation is more pronounced with GRE due to its greater dependence on inflow contrast. In this study, We sought to compare two coronary vein imaging techniques of whole-heart balanced SSFP and a targeted double-oblique spoiled GRE sequence in combination with MT preparation sequence for tissue contrast improvement. MATERIALS AND METHODS CMR imaging was performed on 1.5 Tesla (T) Philips Achieva scanner (Philips Healthcare, Best, Netherlands) equipped with a 16-channel receiver and a 32-
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Figure 1. The imaging sequence used for GRE and SSFP acquisition is shown. Contrast is enhanced by eight off-resonant magnetization transfer preparation pulses (MTC) followed by a navigator (NAV) for tracking of the breathing motion. A fat saturation pulse (FatSat) is applied in front of the imaging sequence (Image) for suppression of fat signal.
element cardiac phased-array coil (InVivo Corporation, Gainesville, FL) combined to a 16-channel receiver using combiner hardware (InVivo Corporation). Written informed consent was obtained from all participants, and the protocols were approved by the hospital Committee on Clinical Investigations. Nine healthy subjects (five males, age 21.1 ⫾ 2.4 years) were scanned with both targeted and whole-heart coronary vein acquisitions. All acquisitions were synchronized to the subjects heartbeat using a vector ECG (14). A scout scan was initially acquired for localization and navigator positioning using a multislice 2D SSFP acquisition (15). Subsequently, an image acquisition was performed to calculate the coil sensitivity maps for parallel imaging (16). A pencil beam navigator, placed on the interface of the lung and the right hemidiaphragm, was used to monitor and gate respiratory motion. A navigator gating window of 5 mm with adaptive drift shifting was used for both whole-heart and the targeted acquisitions. All coronary vein images were obtained during the systolic rest period when coronary veins are maximally dilated (4). This optimal trigger time was visually determined using a breath-hold 2D cine SSFP image in two-chamber orientation with the following imaging parameters: TE ⫽ 1.3 ms, TR ⫽ 2.6 ms, ␣ ⫽ 60°, field of view (FOV) of 320 ⫻ 320 ⫻ 8 mm3, spatial resolution of 2 ⫻ 2 ⫻ 8 mm3, a temporal resolution of 21 ms and a total duration of 10.2 s. The trigger time was then visually selected as the onset of the least-motion period in the cross-section of coronary sinus. Whole-heart coronary vein acquisitions were performed using a magnetization-prepared 3D SSFP sequence (4). Figure 1 shows the used pulse sequence. To improve myocardium blood contrast, an MT preparation sequence was applied before imaging (4,17,18) followed by the navigator for tracking of breathing motion and a fat saturation pulse to suppress fat signal. A series of eight off-resonance pulses with flip angle of 800° and duration of 20 ms each pulse with an offresonance frequency of 500 Hz was used for MTC preparation. The SSFP imaging parameters were as follows: TE ⫽ 2.3 ms, TR ⫽ 4.6 ms, ␣ ⫽ 90°, bandwidth of 769.2 Hz, FOV of 310 ⫻ 310 ⫻ (112–128) mm3, and 75– 85 slices with 3-mm thickness (reconstructed to 1.5 mm after zero-padding). The 20 –25 phase encodings per heartbeat were acquired with a total acquisition of ⬃92– 115 ms per heartbeat. The spatial resolution was 1.2 ⫻ 1.2 ⫻ 3 mm3 reconstructed to 0.54 ⫻ 0.54 ⫻ 1.5 mm3 using zero-padding. The images were acquired and re-
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Figure 2. Example coronary vein images acquired using two targeted acquisitions: along coronary sinus (CS; a– e) and parallel to the lateral wall (f–j). Branching points of coronary veins draining into the CS can be detected. The arrows show the posterior interventricular vein (PIV), the posterior lateral vein (PLV) and the CS. a– e: In this orientation, only a short segment of the branching coronary veins can be seen. f–j: However, in this orientation, take-off points, and angles of branches draining into the CS on the lateral wall can be seen easily without a need for reformatting or multiplanar reconstruction.
constructed using an acceleration factor of 2 with SENSE reconstruction (16). The total acquisition time for the whole-heart imaging, not considering navigator efficiency, was approximately 4 min, assuming a heart rate of 60 beats per minute. In all subjects, whole-heart imaging was followed by two targeted coronary vein acquisitions with different imaging orientation for comparison. Initially, a double oblique 3D imaging protocol was performed along the coronary sinus, prescribed using a 3-point tool positioned with points located at the ostium, and middle and great cardiac vein (CS slab). A perpendicular 3D slab was then prescribed from this acquisition to image the lateral left ventricular wall which shows the lateral branch in the imaging plane for easier visualization (LW slab). For prescription of the two targeted acquisitions the whole-heart dataset was used. Imaging parameters for both GRE scans were as follows: TE ⫽ 1.5 ms, TR ⫽ 5 ms, ␣ ⫽ 30°, and 25 slices (3 mm interpolated to 1.5 mm). The spatial resolution for targeted acquisitions was similar to the whole-heart acquisition: 1.2 ⫻ 1.2 ⫻ 3 mm3 reconstructed to 0.54 ⫻ 0.54 ⫻ 1.5 mm3 with the same SENSE acceleration factor of 2. The acquisition time for each acquisition, not considering navigator efficiency, was approximately 1.5 min.
the left marginal vein (LMV), and the anterior interventricular vein (AIV) were identified. The branching angle between the CS and PLV was measured by using an angle measurement toolkit in the ViewForm software. Measurements in the whole-heart images and the CS slab were made in coronal multiplanar reconstructed views for in-plane viewing of the CS and the lateral vein branches. Images from the LW slab did not require multiplanar reconstruction for measurements. All images were scored by an experienced cardiologist for overall image quality, SNR, contrast between venous blood and myocardial muscle, artifact in the CS, and artifact elsewhere. The images received a score of 1 in each category: if image quality was good, SNR was adequate, contrast was good, no artifacts were detected in the CS or elsewhere on the images. The images received a score of 0 in each category if the above was not true. The total score per acquisition method was summed and averaged over all subjects, with higher total score indicating better image quality. Images were analyzed separately for each imaging method to avoid bias in results from reviewing other images on the same subject. The measured data of both targeted acquisitions was compared separately with the data measured in whole-heart acquisitions using a Wilcoxon signed rank test.
Image Analysis The raw images were viewed and analyzed with Philips ViewForum (Philips Healthcare, Best, NL). For a better assessment of the coronary veins, multiplanar reconstruction was used for whole-heart datasets and targeted CS-slap acquisitions. Anatomical feature assessment and subjective image scoring were performed on whole-heart and targeted acquisitions. The G-factor maps and noise maps (16) were not available, therefore absolute SNR/CNR values were not calculated for parallel image reconstruction. All visible components of the coronary venous system including the coronary sinus (CS), the posterior interventricular vein (PIV), the posterior lateral vein (PLV),
RESULTS Figure 2 shows five slices (Fig. 2a– e) taken from a CS slab targeted acquisitions and five slices (Fig. 2f–j) from an LW slab targeted acquisition from the same subject. The PIV, PLV, and CS can be detected and are marked by arrows. In the CS-slab slice orientation (Fig. 2a– e) the take-off points of branches draining into the CS can be identified. However, it does not cover the entire course of these branches. In the LW slab orientation (Fig. 2f–j), the course of the PIV and the PLV are completely covered and, therefore, can be followed in entirety. The arrows mark the PIV, PLV, and CS. Figure 3
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Figure 3. a–i: Example basal to apical slices extracted from whole-heart datasets of the subject shown in Figure 2. The arrows shows the posterior interventricular vein (PIV), the posterior lateral vein (PLV), the coronary sinus (CS), the left marginal vein (LMV), the anterior interventricular vein (AIV), and the left anterior descending coronary artery (LAD). All branches seen in the targeted acquisition can be identified in whole-heart acquisition in addition to branches mainly located in the anterior wall. However, due to its axial orientation, the identification of CS tributaries and their take-off angle, location, and path is more challenging.
shows nine slices taken from a whole-heart acquisition, prescribed in axial (transverse) orientation, from the same subject shown in Figure 1. The slices are shown in feet to head direction (Fig. 3a–i). The arrows point to the PIV, PLV, CS, AIV, and the LAD. Figure 4 shows the reformatted coronary vein images from a healthy subject reconstructed from a whole-heart dataset (Fig. 4a,c) and a targeted dataset (Fig. 4b,d). The whole-heart dataset was multiplanar reconstructed in lateral wall, similar to the targeted acquisition orientation. The arrows show the PIV, the PLV, and the CS. CS tributaries and their take-off angle can easily be identified. The targeted acquisition yield images with higher overall image quality and less blurring in the plane where CS branches are located. The angle between the PLV and the CS was measured to be 106 ⫾ 17° in the whole-heart acquisitions, 114 ⫾ 23° (P ⫽ 0.25 whole-heart versus LW slab) in the targeted acquisitions covering the lateral wall and 114 ⫾ 15° in the targeted acquisition following the course of the CS (P ⫽ 0.46 whole-heart versus CS slab).
Table 1 summarizes the evaluation of the two imaging approaches in terms of visibility of different coronary branches. The CS was visible in all subjects in the whole-heart as well as both targeted coronary vein acquisitions. Two subjects had no PLV in whole-heart or targeted acquisitions, but the LMV was identified in one of these subjects. The absence of a branch in all three acquisitions was considered to have anatomical reasons. In four subjects (44%), the LMV was identified on whole-heart acquisitions, but not on the targeted acquisitions. Only one subject showed the LMV on all images. There were no cases in which the LMV could be identified on the targeted acquisitions but not on whole-heart images. Between the two orientations of targeted acquisitions, no difference could be seen regarding identification of the LMV. The result of image quality analysis is presented in Table 2. The cumulative score for each acquisition is 3.9 ⫾ 1.3, 3.7 ⫾ 1.2 (P ⫽ 0.67 whole-heart versus CS slab) and 4.8 ⫾ 0.4 (P ⫽ 0.08 whole-heart versus LW slab) for whole-heart, CS, and LW slab, respectively.
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artifacts were identified in the close vicinity of the coronary sinus that could impact the visualization of the coronary vein anatomy. The targeted CS slab shows the lowest contrast, which is potentially associated with higher inflow saturation that is caused from the vessel being located in the imaging plane.
DISCUSSION
Figure 4. Reformatted coronary vein images from a healthy subject reconstructed from a whole-heart dataset (a,c) and a targeted dataset (b,d). The whole-heart dataset was multiplanar reconstructed in lateral wall orientation, similar to the targeted acquisition. The arrows show the posterior interventricular vein (PIV), the posterior lateral vein (PLV), and the coronary sinus (CS). CS tributaries and their take-off angle can easily be identified. The targeted acquisition yield images with higher overall image quality and less blurring in the plane where CS branches are located.
The LW targeted acquisition has the highest image quality with no visible artifacts, although results are not statistically significant for the number of subjects used in this study. Whole-heart images showed artifacts (mainly signal void) outside the coronary veins in four cases (44%). These artifacts were mainly located in the liver and the right atrium. In rare cases, signal voids were found on the inferolateral wall of the heart. No
In this study, we investigated a noncontrast MT prepared 3D SSFP whole-heart sequence to image the coronary veins. To improve the inherent SSFP blood myocardium contrast, an MT preparation sequence was used for whole-heart coronary vein imaging. The images were compared with two targeted, small slab 3D GRE image acquisitions. The whole-heart acquisition has better coverage of the coronary vein anatomy, especially in the anterior walls, because of its larger slab size. However, the assessment and visualization of the branches perpendicular to the imaging plane (axial orientation) is more difficult with the whole-heart acquisition. The multiplanar reconstruction parallel to the lateral wall is the best orientation to evaluate the branches located on the lateral wall in whole-heart. However, the anisotropic resolution and necessity of multiplanar reconstruction to visualize the main coronary vein branches leads to lack of clear identification of branching points and course. A decrease in slice thickness for achieving isotropic resolution leads to SNR loss and increased acquisition time. For LW targeted slab, the images are acquired with the branches mainly localized in the imaging plane, therefore, no multiplanar reconstruction is needed. The whole-heart image acquisition was longer than each targeted acquisition. This prolonged acquisition could result in failure in completion of the study due to respiratory drift with poor navigator efficiency. Furthermore, evaluation of the patients with heart failure requires not only the assessment of coronary vein anatomy but also other clinical relevant information such as ventricular viability, function, and mechanical dyssynchrony. Therefore, acquisition speed in coronary vein assessment is very important. Although the use of 2D parallel imaging could further accelerate the wholeheart imaging acquisition, this technique still faces challenges due to SNR degradation. Its potential lies in the ease of image planning, which may lead to potential advantages in clinical use.
Table 1 Visual Assessment of the Presence of Different Coronary Vein Branches in Whole-Heart and Targeted Acquisitions* Coronary vein branch
Whole-heart [%]
Targeted (CS-orientated) [%]
Targeted (LW-orientated) [%]
Coronary sinus (n⫽9) Posterior lateral (n⫽7) Posterior interventricular ( n⫽9) Anterior interventricular (n⫽9)
100 100 89 100
100 100 56 (P⫽0.08) 78 (P ⫽N.S.)
100 86 (p⫽N.S.) 78 (p⫽N.S.) 100
*If subjects showed no posterior lateral branches on any of three scans, this branch was considered to be anatomically absent. Wilcoxon signed rank test was used to compare each small slab targeted acquisition to the whole-heart acquisition. CS ⫽ coronary sinus; LW ⫽ lateral left ventricle wall; N.S., not significant.
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Table 2 Visual Grading of Coronary Vein Images for Each Acquisition Type* Visual grading
Whole-heart
Targeted (CS-orientated)
Targeted (LW-orientated)
Overall image quality SNR Contrast Artifacts in the CS Artifacts elsewhere Average score
7 9 5 9 5 3.9
5 (P ⫽ N.S.) 8 (P ⫽ N.S.) 3 (P ⫽ N.S.) 9 8 (P ⫽ N.S.) 3.7 (P ⫽ N.S)
9 (P ⫽ N.S.) 9 7 (P ⫽ N.S.) 9 9 (P ⫽ 0.05) 4.8 (P ⫽ 0.08)
*Each dataset was scored based on the criteria listed in the first column. The scores ranged from 0 (bad / significant artifacts) to 9 (excellent / no artifacts). Average score per image over all subjects was calculated. The Wilcoxon signed rank test was used to compare each small slab targeted acquisition to the whole-heart acquisition. CS ⫽ coronary sinus; LW ⫽ lateral left ventricular wall; SNR ⫽ signal-to-noise ratio; N.S., not significant.
STUDY LIMITATIONS We did not compare contrast-enhanced techniques to our noncontrast-based imaging approach proposed in this study. A contrast agent-based approach is subject to several limitations. Coronary imaging with extravascular contrast agents is very challenging due to the limited time window available for imaging before contrast washout. It has been shown that the use of gadobenate dimeglumine ([Gd-BOPTA]2⫺) as an extracellular contrast agent at slow injection rates is feasible for whole-heart coronary artery imaging (19). Further study to investigate slow infusion imaging using this contrast agent for coronary vein imaging is required to demonstrate the feasibility of this technique. Use of an intravascular contrast agent of B-22956/1 (Bracco Imaging SpA, Milan, Italy) has been reported for coronary vein imaging (5). However, this contrast agent is not currently FDA approved in the United States. In CHF patients undergoing CMR assessment, a late gadolinium-enhanced viability scan with gadolinium-based extracellular contrast agent is frequently clinically indicated. Administration of two contrast agents (one intravascular and one extravascular) within a single imaging session is not likely to be feasible in clinical practice. Therefore, a noncontrast method for coronary vein imaging is preferred. Use of alternative sampling trajectory such as spiral sequences for whole-heart coronary vein MRI might be beneficial (20). This has, however, not been explored in this study. In this study, we have used parallel imaging to reduce acquisition time for both whole-heart and targeted acquisition to enable completion of the study in a single CMR scan. CNR and SNR calculations require the acquisition of a g-factor map (16). The g-factors were not reconstructed in this study, therefore, we were not able to measure and report CNR or SNR comparison between the two acquisitions. The minimal spatial resolution in CMR evaluation of coronary vein anatomy has not been investigated previously. In this study, we used a nominal acquired resolution of 1.2 ⫻ 1.2 ⫻ 3 mm3 in whole-heart acquisition. The spatial resolution was determined in a series of initial studies in which images were acquired for evaluation of image quality. Acquired slice thickness was changed from 1.5 mm to 3 mm in five additional subjects to this study. Our preliminary attempts in image acquisition with a thinner slice thickness (1.5
mm reconstructed to 0.75 mm) resulted in failure secondary to long acquisition time and significant image artifacts around the coronary veins due to longer TR (5.2 ms). Acquired in-plane spatial resolution was also varied from 1.0 mm to 1.6 mm in five subjects. At higher spatial resolution, significant image artifacts were seen due to longer TR in SSFP. To be able to perform a fair comparison between targeted and whole-heart acquisition, in plane resolution of the targeted GRE acquisition was reduced compared with previous studies (4). In this study, we did not compare a whole-heart SSFP with a lower spatial resolution-targeted SSFP imaging sequence that could potentially have less banding artifact due to lower TR. Shorter excitation pulses could be used to reduce TR and, therefore, reduce image artifacts due to off-resonance in the SSFP sequences at the cost of worsened excitation slab profiles. The effect of shorter excitation pulses for 3D SSFP sequences on the signal intensity and the tissue contrast needs to be investigated further. In this study, we used the three-point tool on the data acquired from whole-heart acquisition for planning of the targeted imaging slabs. A lower spatial resolution images similar to one commonly used for coronary arteries can be used to prescribe the targeted images as well. However, an acquisition in the coronary sinus slab is required for prescription of the LW wall. In conclusion, we have demonstrated the feasibility of noncontrast SSFP whole-heart coronary vein imaging using magnetization transfer sequence. The comparison between whole-heart 3D SSFP acquisitions and small slab targeted GRE acquisitions showed that the targeted acquisition covering the lateral wall is superior and easier for visualizing the branches important to cardiac resynchronization therapy. ACKNOWLEDGMENT This work was supported in part by a grant from the American Heart Association (AHA SDG-0730339N). REFERENCES 1. Cleland JG, Daubert JC, Erdmann E, et al. The effect of cardiac resynchronization on morbidity and mortality in heart failure. N Engl J Med 2005;352:1539 –1549. 2. Abraham WT, Fisher WG, Smith AL, et al. Cardiac resynchronization in chronic heart failure. N Engl J Med 2002;346:1845–1853.
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