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Echocardiographic Phase Imaging to Predict Reverse Remodeling After Cardiac Resynchronization Therapy

Sebastian J. Buss, MD^_*,_*, Per M. Humpert, MD, Raffi Bekeredjian, MD^_*, Stefan E. Hardt, MD^_*, Christian Zugck, MD^_*, Dieter Schellberg, PhD^,, Alexander Bauer, MD^_*, Arthur Filusch, MD^_*, Helmut Kuecherer, MD^||, Hugo A. Katus, MD^_*, Grigorios Korosoglou, MD^_*

^_* Department of Cardiology, University of Heidelberg, Heidelberg, Germany
Department of Endocrinology, University of Heidelberg, Heidelberg, Germany
Department of Visceral and General Surgery, University of Heidelberg, Heidelberg, Germany
Department of Psychosomatic and General Internal Medicine, University of Heidelberg, Heidelberg, Germany
^|| Department of Cardiology, Kliniken im Naturpark Altmühltal, Eichstätt, Germany

	Abstract

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Objectives: The aim of our study was to investigate whether echocardiographic phase imaging (EPI) can predict response in patients who are considered for cardiac resynchronization therapy (CRT).

Background: CRT improves quality of life, exercise capacity, and outcome in patients with bundle-branch block and advanced heart failure. Previous studies used QRS duration to select patients for CRT; the accuracy of this parameter to predict functional recovery, however, is controversial.

Methods: We examined 42 patients with advanced heart failure (New York Heart Association [NYHA] functional class III to IV, QRS duration >130 ms, and ejection fraction <35%) before and 6 to 8 months after CRT. Left ventricular (LV) dyssynchrony was estimated by calculating the SD of time to peak velocities (Ts-SD) by conventional tissue Doppler imaging (TDI), and the mean phase index (mean EPI-Index) was calculated by EPI in 12 mid-ventricular and basal segments. Patients who were alive and had significant relative decrease in end-systolic LV volume of ESV 15% at 6 to 8 months of follow-up were defined as responders. All others were classified as nonresponders.

Results: The Ts-SD and the mean EPI-Index were related to ESV (r = 0.43 for Ts-SD and r = 0.67 for mean EPI-Index, p < 0.01 for both), and both parameters yielded similar accuracy for the prediction of LV remodeling (area under the curve of 0.87 for TDI vs. 0.90 for EPI, difference between areas = 0.03, p = NS) and ejection fraction (EF) improvement (area under the curve of 0.87 for TDI vs. 0.93 for EPI, difference between areas = 0.06, p = NS). Furthermore, patients classified as responders by EPI (mean EPI-Index 59%) showed significant improvement in NYHA functional class and in 6-min walk test (409 ± 88 m at follow-up vs. 312 ± 86 m initially, p < 0.001).

Conclusion: Echocardiographic phase imaging can predict functional recovery, reverse LV remodeling, and clinical outcomes in patients who undergo CRT. EPI is a method that objectively and accurately quantifies LV dyssynchrony and seems to be noninferior to TDI for the prediction of reverse LV remodeling and functional recovery.

Key Words: cardiac resynchronization therapy • congestive heart failure • echocardiographic phase imaging • left ventricular dyssynchrony • tissue Doppler imaging

Abbreviations and Acronyms   CRT = cardiac resynchronization therapy   EF = ejection fraction   EPI = echocardiographic phase imaging   ESV = end-systolic volume   LV = left ventricle/ventricular   NYHA = New York Heart Association   TDI = tissue Doppler imaging   Ts-SD = SD of time to peak velocities

We have previously reported on the utility of the parametric echocardiographic phase imaging (EPI) for the objective evaluation of LV dyssynchrony in patients with type 2 diabetes mellitus (12,13). In the present study we used EPI to predict reverse remodeling, functional LV recovery, improvement of heart failure symptoms, and clinical outcome in patients who undergo CRT.

	Methods

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Patients.   The study population consisted of 45 consecutive patients who underwent clinically indicated CRT due to the following criteria: 1) congestive heart failure (New York Heart Association [NYHA] functional class III/IV) for at least 12 months due to dilative (n = 24) or ischemic (n = 18) cardiomyopathy; 2) wide QRS complex (>130 ms) of left bundle branch block-like morphology; and 3) severely impaired LV function (ejection fraction <35%). Patients with acute ischemic syndromes or revascularization within the previous 6 months were excluded. The study protocol was approved by the local ethics committee, and all subjects gave written informed consent.

Echocardiography.   Three of 45 consecutive patients were excluded from the study due to poor echogenic windows, so that our study population consisted of 42 patients. Patients were studied with a commercially available ultrasound system (Acuson, Sequoia, Mountain View, California), with a 4.25-MHz transducer and simultaneous electrocardiographic recording. Imaging was performed in standard parasternal long- and short-axis and in apical 2-, 3-, and 4-chamber view. All data were acquired during breath-hold to minimize translation movement of the heart. Ejection fraction and end-systolic and end-diastolic LV volumes were quantified with the biplane Simpson's method (13). Follow-up echocardiography was performed 6 to 8 months after CRT.

Evaluation of dyssynchrony.   Standard deviation of time-to-peak systolic velocities by TDI
The TDI was acquired from the apical 2-, 3-, and 4-chamber views with high frame rate (>80/s). The TDI measurements were assessed in 12 basal- and mid-ventricular segments from the apical 2-, 3-, and 4-chamber view to evaluate longitudinal function. Regions of interest were manually placed during systole, and myocardial velocities were measured with commercially available software (Research Arena, TomTec Imaging Systems GmbH, Munich, Germany) (12,13). Myocardial velocity curves were obtained and the time to peak velocity during ejection phase (Ts) was measured in each segment. To assess global LV synchronicity, the SD of Ts of all 12 segments (Ts-SD) was computed (9). High Ts-SD values correspond to high LV dyssynchrony and vice versa.

Mean phase index by EPI
Ventricular contraction and relaxation result in cyclic changes in gray level intensities of picture elements (pixels) that are encompassed by the moving endocardial border during the cardiac cycle. These changes in signal intensity are mathematically transformed with a first harmonic Fourier algorithm. EPI has been validated in previous studies to evaluate regional wall dyssynergy, by displaying contraction sequence and magnitude with high reproducibility (12–14). By this algorithm time-intensity curves of each individual image pixel are fitted to a first harmonic curve, which is characterized by its phase angle and amplitude. Hereby, the amplitudes are related to pixel intensity, whereas the phase angles are related to the onset and timing of pixel intensity change. With EPI, phase angles are automatically transformed into intensity parameters and displayed in shades of gray, which are related to the amplitude of the structure analyzed. Applied to endocardial surfaces and chamber walls, the phase angle relates to the sequence of wall thickening and motion of the endocardium. The spectrum of gray levels is then color encoded with a pre-defined cyclic scale (14). By that, the color phase image displays the relative timing of intensity change of image pixels in a "composite" parametric format. Because maximal endocardial inward motion is expected to occur during the relatively early ejection period, normal systolic endocardial inward motion yields phase angles near the end 360° or start 0° (green color shades), while inverted and triphasic displacement curves (e.g., with paradoxical septal wall motion) have phase angles near (180°) of the cardiac cycle (red color shades). Because 360° represent the length of a complete heart cycle, phase differences of 0° or 360° indicate perfect synchrony, whereas differences of 180° indicate maximal dyssynchrony of contraction.

To quantify LV dyssynchrony, digitized echocardiographic loops were used, which were gated at the peak of the R-wave. Endocardial borders were manually drawn in end-systolic frames, and regions of interest were generated automatically with a fixed width of 4 mm (Research Arena, TomTec), which automatically track the endocardial motion throughout the whole cardiac cycle. Phase values for each image pixel were displayed in composite parametric images (Figs. 1A, 1C and 1E), and gray-scale intensities were plotted versus time (Figs. 1B, 1D, and 1F). Echocardiographic phase indexes (EPI-indexes) were computed for each segment, by relating the extent of local dyssynchrony to that of all the other segments of the LV. To assess global cardiac synchronicity, the mean value of the EPI-indexes of 12 basal- and mid-ventricular segments from the apical 2-, 3-, and 4-chamber view was calculated (mean EPI-index). Low values of the mean EPI-Index correspond to high LV dyssynchrony and vice versa. Figure 1 illustrates the parametric images of a healthy volunteer (Figs. 1A and 1B) with relatively coordinated wall motion (septal and lateral segments coded green). Conversely, in a patient scheduled for CRT due to ischemic cardiomyopathy, regional dyssynchrony in contraction can be appreciated in the corresponding images (Figs. 1C and 1D). Thus, lateral wall (segments 3 and 4) occurs much later than septal contraction (segments 1 and 2, coded red in the parametric image) (Fig. 1C). Six months after CRT in the same patient all septal and lateral myocardial segments are coded green (Fig. 1E), implying re-coordinated wall motion (Fig. 1F).

View larger version (66K): [in this window] [in a new window] [Download PPT slide]   Figure 1 Examples for EPI (A and B) Echocardiographic phase imaging (EPI) in a healthy subject with normal wall motion (septal and lateral segments coded green). (C and D) An EPI in a patient with advanced heart failure, who demonstrates regional dyssynchrony in contraction. Contraction of the lateral wall (segments 3 and 4) occurs much later than maximal septal contraction (segments 1 and 2, coded red in the parametric image) (C). (E and F) Six months after cardiac resynchronization therapy nearly the whole myocardium is now coded green (E), implying re-coordinated wall motion (F). The corresponding original images, before removal of the left ventricular cavity for better endocardial definition, are displayed in small white boxes beside the main images.

Definition of CRT responders and end points.   Patients were divided into 2 groups according to their response to CRT. Patients with significant reverse LV remodeling (relative decrease of LV systolic volume [ESV] of 15%) (16) were defined as responders (primary end point). Patients were defined as nonresponders if they died due to cardiac causes or did not reach the pre-defined echocardiographic change in ESV at 6 to 8 months of follow-up. Furthermore, we used the absolute increase in LV ejection fraction of 0.08 (8%) versus baseline (EF >8%) (17,18) as an additional end point of our study. Functional assessment was performed initially and at follow-up and included NYHA functional class and 6-min walk distance test. These variables were associated with baseline LV dyssynchrony and deemed as secondary end points of our study. All end points were assessed at 6 to 8 months of follow-up.

Statistical analysis.   Data are presented as mean ± SD. Intraobserver and interobserver variability and time spent for the estimation of TDI and EPI parameters were obtained by repeated analysis of 20 representative images. Differences in baseline characteristics between responders and nonresponders and differences in variables between the initial and the follow-up visit were evaluated by unpaired and by paired Student t tests, respectively. The extent of LV dyssynchrony by EPI was compared with that of TDI, with the EF, and with ESV using linear regression analysis. Receiver-operating characteristics were used to assess the predictive value of TDI and of EPI for the primary end points, including functional recovery and LV remodeling. Differences in sensitivities, specificities, and accuracies between EPI and TDI were evaluated with the exact McNemar test. Pair-wise comparison of areas under the curve of receiver operating characteristics curves (19) was assessed with MedCalc8.2 (MedCalc software, Mariakerke, Belgium). Differences were considered significant at p < 0.05.

	Results

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Patient characteristics and response to CRT.   The baseline characteristics of 42 patients included in the study are illustrated in Table 1. At 6 to 8 months of follow-up, 5 patients died due to intractable heart failure. No patient underwent revascularization during the follow-up period. According to pre-defined definitions 26 patients were responders and 16 were nonresponders. Demographic and clinical characteristics and baseline ejection fraction did not significantly differ between responders and nonresponders (Table 1).

View larger version (18K): [in this window] [in a new window] [Download PPT slide]   Figure 2 Correlation of Mean-EPI With Tissue Doppler Imaging Mean echocardiographic phase imaging (EPI)-index correlated inversely with SD of time to peak velocities (Ts-SD) (r = –0.78, p < 0.001).

View larger version (26K): [in this window] [in a new window] [Download PPT slide]   Figure 3 Prediction of Response to CRT by Tissue Doppler and by EPI The extent of baseline dyssynchrony both by SD of time to peak velocities (Ts-SD) and by the mean echocardiographic phase imaging (EPI)-Index was related to reverse remodeling (A and B) and to functional recovery (E and F). The Ts-SD and mean EPI-Index showed similar diagnostic characteristics for the prediction of remodeling (C and D) and functional recovery (G and H) (cutoff values selected within our study cohort [solid arrows] and as proposed by Yu et al. [20] [hatched arrows] can be appreciated in C, D, G, and H). AUC = area under the curve; CRT = cardiac resynchronization therapy; EF = ejection fraction, ESV = end-systolic volume; LV = left ventricular.

Association of baseline LV dyssynchrony with NYHA functional class improvement and with 6-min walk test.   Of 26 patients classified as CRT responders (EPI-index 59% at baseline), 1 died due to intractable heart failure, and 21 (84%) of the 25 remaining patients showed improvement of heart failure symptoms. Of 16 patients classified as nonresponders by EPI, 4 died due to heart failure, and only 3 of the remaining 12 patients (25%) showed improvement of heart failure symptoms (Figs. 4A and 4B). In addition, CRT responders showed significant improvement in 6-min walk test at follow-up, in contrast to patients who were classified as nonresponders by EPI (312 ± 86 m initially vs. 409 ± 88 m at follow-up for responders, p < 0.001, and 304 ± 90 m initially vs. 327 ± 93 m at follow-up for nonresponders, p = NS) (Figs. 4C and 4D).

View larger version (25K): [in this window] [in a new window] [Download PPT slide]   Figure 4 Association of Baseline Left Ventricular Dyssynchrony With NYHA Functional Class Improvement and With 6-min Walk Test (A and B) Cardiac resynchronization therapy (CRT) responders showed significant improvement of New York Heart Association (NYHA) functional class. (C and D) The CRT responders by echocardiographic phase imaging (EPI) showed significant improvement in 6-min walk test at follow-up, in contrast to those classified as nonresponders by EPI. Indicates death due to intractable heart failure.

	Discussion

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To our knowledge this is the first study to report the usefulness of EPI to predict functional recovery, reverse LV remodeling, and clinical outcomes in patients who undergo CRT. EPI can objectively and easily quantify LV dyssynchrony with higher reproducibility and significantly lower time spent compared with TDI. In light of the modest diagnostic performance and the high observer variability of TDI to predict response to CRT (11), these findings now warrant the initiation of multi-center clinical trials, to investigate the ability of EPI as a new screening tool for patients who are considered for CRT.

TDI has emerged as an echocardiographic method that uses color-coding of myocardial velocity to quantify regional alterations in myocardial contractility (9,10,20,21). Recently, TDI was successfully used to measure timing of longitudinal myocardial contraction velocities (22). Hereby, the extent of intersegmental differences in time to peak systolic velocities (Ts) and systolic strain was closely related to functional recovery of patients who underwent CRT (8,9,17,20). However, TDI is limited to the study of longitudinal axis motion due to practical grounds, given available windows for transducer placement. For this reason and because myocardial contraction principally occurs in the radial direction, TDI might be less sensitive for LV dyssynchrony assessment compared with methods that evaluate radial motion (23,24).

EPI is an echocardiographic technique that uses a first harmonic Fourier algorithm to measure the magnitude and timing of myocardial deformation in the circumferential direction. This technique has been previously used to quantify wall motion dyssynchrony in patients who undergo CRT for advanced heart failure (25), predicting acute hemodynamic benefits. However, to our knowledge this is the first study to report the usefulness of EPI to predict functional recovery, reverse remodeling, and benefits on exercise capacity and on heart failure symptoms. The accuracy of EPI to predict functional recovery and reverse remodeling in patients who undergo CRT was similar to that provided by TDI. Thus, patients classified as CRT responders by EPI had significant improvement of heart failure symptoms and of their functional capacity. Furthermore, the assessment of LV dyssynchrony by EPI was less time-consuming compared with TDI and had low observer variability, in agreement with previous reports (13). The less time spent on EPI compared with conventional TDI techniques was attributed to the automatic depiction of myocardial segments by EPI, whereas placement of regions of interest by TDI was assessed manually and was often technically challenging in nonbasal LV segments.

Study limitations.   The present study included a relatively small number of patients, which might have skewed the receiver operating curve analysis and the estimation of sensitivity and specificity parameters. In this regard, selecting a cutoff value of 32 ms, as suggested by Yu et al. (20), provided high sensitivity but relatively low specificity for the prediction of LV remodeling in our group. Future studies should include larger numbers of patients in order to evaluate the predictive value of this method on long-term clinical outcomes and mortality. EPI cannot distinguish between active contraction and passive myocardial motion, which might prevent the identification of scarred myocardium in the region of the tip of the LV pacing lead with this technique. Conversely, with speckle tracking (24) or tagged magnetic resonance (23,26), 2-dimensional strain and radiofrequency pulses are used to track echocardiographic speckles and tags of the myocardium, respectively. These techniques measure active myocardial contraction and provide the assessment of regional differences in radial/circumferential strain with high accuracy. Furthermore, EPI was not used to locate the area of latest activation or to evaluate effects of immediate resynchronization in our study, although this is technically feasible. Matching the LV lead position with the site of latest mechanical activation might be necessary for CRT response, as recently reported by Van de Veire et al. (27). This technique might therefore be useful in future studies in order to guide positioning of the LV lead, by assessing the sequence of wall thickening and motion of the endocardium.

	Conclusions

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Echocardiographic phase imaging can predict functional recovery, reverse LV remodeling, and clinical outcomes in patients who undergo CRT. Thus, EPI can be implemented in busy echocardiographic laboratories to quantify LV dyssynchrony and to correctly select patients considered for CRT treatment with high accuracy.

	Footnotes

 
This study was supported by grants from the German Society of Cardiology (to Dr. Korosoglou).

^_* Reprint requests and correspondence: Dr. Sebastian J. Buss, University of Heidelberg, Department of Cardiology, Im Neuenheimer Feld 410, 69120 Heidelberg, Germany (Email: sebastian.buss{at}med.uni-heidelberg.de).

Manuscript received July 2, 2008; revised manuscript received March 6, 2009, accepted March 10, 2009.

	REFERENCES

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