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European Journal of Heart Failure 2002 4(1):41-48; doi:10.1016/S1388-9842(01)00205-7
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© 2002 European Society of Cardiology

Prognostic implication of myocardial texture analysis in idiopathic dilated cardiomyopathy

Bahadir Dagdevirena,*, Osman Akdemirb, Mehmet Erena, Osman Bolcaa, Enis Oguza, Yekta Gürlertopa and Tuna Tezela

a Siyami Ersek Thoracic and Cardiovascular Surgery Center, Cardiology Clinic Istanbul, Turkey
b Trakya University, School of Medicine, Cardiology Department Edirne, Turkey

* Corresponding author. Acibadem cad. Nisantasi duragi, Pitrak sok. No: 20/B 81010 Üsküdar, Istanbul, Turkey. Tel.: +90-216-3265181; fax: +90-216-3265181. E-mail address: bahadird{at}superonline.com


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Background and aim: Abnormal myocardial acoustic properties have been reported in patients with idiopathic dilated cardiomyopathy (IDC). The aim of this study was to investigate the relationship between quantitative ultrasonic textural alterations of myocardium and clinical outcome in IDC.

Methods: Baseline clinical and echocardiographic variables were obtained from 28 patients with IDC. By using a videodensitometric approach, quantitative myocardial texture analysis was performed on images obtained from septum and posterior wall (PW). Cyclic variation (CV) index of mean gray level (MGL) was calculated according to the formula: (MGLdiast–MGLsyst)/MGLdiastx100. All patients were followed for an average of 11±5 months for the occurrence of cardiac death or repeated hospitalization due to worsening of heart failure.

Results: During follow-up, 10 patients experienced cardiac events (6 cardiac deaths and 4 heart failure events). The CV indexes of both septum and PW were significantly lower in patients with cardiac events than those of event free patients (6.8±9.6% vs. 13.6±8.2%, P<0.05 and 5.3±6.4% vs.15.7±7.2% P<0.001, respectively). Univariate analysis defined the following variables as predictors of outcome: PW–CV index ({chi}2=13.0, P=0.0003), transmitral E/A ratio ({chi}2=12.5, P=0.0004), symptom status ({chi}2=8.7, P=0.003), and septum-CV index ({chi}2=4.7, P=0.03). Multivariate stepwise regression analysis showed that the PW–CV index ({chi}2=7.5, P=0.006) and E/A ratio ({chi}2=6.5, P=0.01) were the independent predictors of outcome. The event-free survival rate of patients with PW–CV index <11% was significantly lower than those with an index ≥11 (35.7% vs. 92.8%, P=0,001).

Conclusion: The assessment of severely depressed CV index provides valuable prognostic information in patients with IDC.

Key Words: Idiopathic dilated cardiomyopathy • Myocardial texture analysis • Prognosis

Received January 18, 2001; Revised April 25, 2001; Accepted August 14, 2001


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
It would be desirable to identify additional echocardiographic indices for predicting the clinical outcome of patients with idiopathic dilated cardiomyopathy (IDC), which is a disease with variable natural history. Ultrasonic tissue characterization has been proposed as a method defining the physical state of the myocardium beyond the chamber dimensions and functional indexes assessed by conventional two-dimensional (2D) echocardiography [1,2]. The videodensitometric method has been successfully applied to demonstrate the alterations of myocardial textural parameters in a variety of pathologic conditions including myocardial ischemia [3,4], left ventricular hypertrophy [5,6], amyloidosis [7], hypertrophic, and dilated cardiomyopathy [8–10].

Increased myocardial echo intensity and decreased cyclic variation of backscattered ultrasound have previously been reported in patients with IDC [9–11]. However, in some patients with IDC, nearly normal myocardial acoustic properties have also been demonstrated [12]. Furthermore, it has been shown that the group of patients with relatively preserved acoustic properties had more likely benefit from beta-blocker therapy [13]. Our study was designed to investigate whether the altered acoustic properties by means of videodensitometric analysis could provide prognostic information in patients with IDC.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
2.1. Patients
Twenty-eight consecutive patients with IDC (9 women, mean age 52±13 years) who met the following diagnostic criteria were prospectively studied: (1) dilated left ventricle [left ventricular end-diastolic diameter (LVEDD) >60 mm and left ventricular end-systolic diameter (LVESD) >45 mm]; (2) fractional shortening (FS) <25% and ejection fraction (EF)<40%; (3) normal coronary angiographic evaluation; (4) absence of primary valvular disease or regional wall motion abnormality on echocardiography; (5) absence of hypertension and diabetes mellitus; and (6) absence of alcohol abuse, or drug abuse or administration that could potentially affect the myocardium. Exclusion criteria were atrial fibrillation and serious ventricular arrhythmias.

Nine patients were in New York Heart Association (NYHA) functional class II, 12 patients were in class III and seven patients were in class IV. All patients were on medical therapy with digoxin, angiotensin converting enzyme inhibitors and diuretics. Informed consent was obtained from all patients.

2.2. Doppler echocardiography
The examinations were performed using a HP Sonos 1500 system (Hewlett Packard, Andover, MA) with a 3.5-MHz phased-array transducer. The images were recorded on videotapes for later analysis. M-mode measurements of left ventricular dimensions and wall thickness were made according to the recommendations of the American Society of Echocardiography on parasternal long axis view [14]. Left ventricular volumes and ejection fractions were measured by using the modified Simpson method on apical four- and two-chamber images. Pulsed wave Doppler mitral velocity curves were obtained from the apical four-chamber view by positioning a 1-mm sample volume between the tips of the mitral valve leaflets in diastole. The peaks of early (E) and late diastolic (A) velocity curves were measured. The measurements represent the mean of three consecutive cardiac cycles.

2.3. Videodensitometric analysis of myocardial texture
The gain settings and gain compensation profiles of echocardiographic system were adjusted to a point where the interventricular septum and posterior wall myocardial brightness were uniform and clearest for each patient. The gray scale pre-process and post-process functions of the system were set to be linear with 25–30-dB amplification at a depth of 16–20 cm. In all subjects, the optimal end-diastolic and end-systolic 2D echocardiographic images of three consecutive beats were digitized onto a personal computer by using a commercially available video-capture card (Tekram-M205) connected to the S-VHS output of the system, and converted into 384x288 pixels of 256 gray levels each (0=black, 255=white) with 8 bits of intensity range. End-diastole was defined as the point in the cardiac cycle at the onset of the electrocardiographic R wave. End-systole was defined as the time of apparent minimal left ventricular chamber size occurred near the peak of the T wave. The mean gray level (MGL) of a region of interest (ROI) drawn with the help of a mouse and pad was calculated by using dedicated software (UTHSCSA-ImageTool ver.2.0) which enables us to generate a histogram, plotting the gray level distribution on the abscissa and the frequency of occurrence on the ordinate for each ROI (Fig. 1). On the images obtained from the parasternal long axis view, we attempted to place each ROI on the same location of septum and posterior wall (around the level of mitral leaflet tips) by consensus of two observers. Special attention was paid for including only the myocardium and excluding the endocardial and epicardial specular echoes to avoid areas of echo dropouts and obvious artefacts. The MGL of each cavity region was accepted as the background signal and was subtracted from the absolute MGL of the myocardium both at end-systole and end-diastole. The CV index of MGL was calculated according to the formula: (MGL diast–MGL syst)/MGL diastx100 [15]. Two independent observers determined the interobserver variability of the method by comparing 10 randomly selected records. One observer repeating the same analysis 4 weeks later estimated the intraobserver variability. The reproducibility of these measurements was assessed by using linear regression analysis. The intra- and interobserver variations were in acceptable limits both for septum and PW (SEE=6.3 and 7.2% for septum — 5.5 and 5.6% for PW, respectively).


Figure 1
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  		Fig. 1 Cavity corrected mean gray level (MGL) measurement and cyclic variation (CV) index calculation of posterior wall in two patients. The upper panel (a) representing a patient free of event during follow-up. The lower panel (b) representing a patient who died at 3rd month of follow-up due to progressive pump failure. ES, end-systole; ED, end-diastole.

 
2.4. Follow-up
All patients were followed up for at least 12 months unless a major end point terminates the follow-up. Cardiac death and heart failure events (hospitalization requirement due to worsening heart failure) were considered as the end points. Cardiac death was defined as death attributable to congestive heart failure, cardiac arrest, or sudden death (i.e. death from circulatory failure occurring within the first hour after the onset of symptoms). Cardiac death was considered as the primary event if a patient experienced both heart failure event and death. The patients with NHYA-class IV were enrolled into the study if they could be stably discharged from hospital with oral medication. The follow-up data were obtained by outpatient evaluation every 6 months, through telephone interviews in every month and from hospital records.

2.5. Statistical analysis
Continuous variables were expressed as mean±1 S.D. and categorical data as percentages. Continuous and categorical variables of the groups were compared by using Mann–Whitney U and chi-square tests, respectively. Event-free survival curves were estimated by the Kaplan–Meier method, and they were compared with the log rank test. Significance was set at a P value <0.05. The predictors of primary events were investigated by univariate analysis with cox-regression model. Significant predictors (P=0.05) were added to the multivariate stepwise regression model. Backward stepwise selection was then performed to identify independent prognostic factors. SPSS 7.5 was used for computations.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
The mean follow-up duration was 11±5 months, ranging from 2 to 18 months. A total of 10 major events occurred during the follow-up period. Six patients experienced sudden death (n=1) and death from progressive pump failure (n=5). Due to deterioration of symptom status, four patients required repeated hospitalization and all of these patients underwent multichamber pacing while awaiting heart transplantation. The remaining 18 patients completed the follow-up period (at least 12 months) without any event. The event-free curves of cardiac deaths, heart failure events and, cardiac events (cardiac deaths plus heart failure events) are shown in Fig. 2.


Figure 2
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  		Fig. 2 Event-free survival curves of cardiac deaths, heart failure events and cardiac events (cardiac deaths plus heart failure events) in patients with idiopathic dilated cardiomyopathy.

 
Baseline clinical characteristics and the conventional echocardiographic indexes of patients with cardiac events were compared with those of event free patients in Table 1. The rate of being in NYHA class IV was significantly higher among the patients with cardiac events. Although EF, FS and wall thickness were higher, and left ventricular dimensions and volumes were lower in the event-free group, the differences did not reach statistical significance. The mean E/A ratio of patients with cardiac events was significantly higher than those of event-free patients (1.7±0.2 vs. 1.2±0.3, P<0.01).


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  		Table 1 Comparison of baseline clinical and echocardiographic variables between patients with cardiac events (cardiac death and heart failure events) and patients free of event

 
The videodensitometric variables are shown in Table 2. The myocardial diastolic and systolic MGL levels of septum and PW were not significantly different between the groups. On the other hand, patients with cardiac events had significantly lower CV indexes of both septum and PW when compared to event-free patients (6.8±9.6% vs. 13.6±8.2%, P<0.05 and 5.3±6.4% vs. 15.7±7.2%, P<0.001, respectively). Patients with an index <11% — the median CV index value of the study group — had significantly lower 1-year survival estimates than those with an index ≥11% (60.9% vs. 92.8%, P=0.03). The cardiac event-free rate was also significantly lower in patients with PW–CV index <11% than those with an index ≥11% (35.7% vs. 92.8, P=0.001) (Fig. 3).


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  		Table 2 Comparison of myocardial textural measurements between patients with cardiac events and patients free of event

 


Figure 3
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  		Fig. 3 Comparison of cardiac death (a) and cardiac events free survival curves (b) between patients with PW–CV index lower and higher than the median value of 11%.

 
Univariate and multivariate predictors of primary events were displayed in Table 3. Among the clinical, echocardiographic and videodensitometric parameters, PW–CV index ({chi}2=13.0, P=0.0003), transmitral Doppler E/A ratio ({chi}2=12.5, P=0.0004), NHYA functional class ({chi}2=8.7, P=0.003), and septum CV index ({chi}2=4.7, P=0.03) were defined as associating factors with prognosis. The multivariate stepwise regression analysis demonstrated that the PW–CV index and the E/A ratio were significant independent predictors of outcome in this model ({chi}2=7.5, P=0.006 and {chi}2=6.5, P=0.01). In this specific study population, NYHA functional class and septal CV index did not add any additional prognostic power to this model.


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  		Table 3 Univariate and multivariate predictors of cardiac events in patients with idiopathic dilated cardiomyopathy

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
The results of the present study suggest that quantitative myocardial textural parameters provide valuable information on clinical outcome of patients with IDC. Our patients with cardiac events at 1-year clinical follow-up had severely depressed cycle dependent myocardial gray level variation. In addition, in this specific study population with predominantly moderate to severe LV dysfunction due to IDC, the CV index of PW independently associated with cardiac events.

Ultrasonic myocardial tissue characterization was based upon two main subtitles: (1) the absolute level of ultrasound backscattered by the diseased myocardium; and (2) the magnitude of its cyclic variability. Attempts were made to explain cyclic modulation of myocardial-backscattered ultrasound with the mechanisms related to sarcomere shortening (i.e. changes in acoustic impedance, fiber orientation, and elastic modules) [16–18]. Previous observations suggest that an index reflecting this cyclic variability of MGL enables us to differentiate ischemic [19,20], hypertensive [6], and diabetic [21] hearts from normal myocardium, and to discriminate viable myocardium from non-viable scar tissue [15]. Although IDC is among the conditions where the cyclic variation of tissue reflectivity is reduced, Naito et al. demonstrated nearly normal textural parameters in approximately one-quarter of patients when compared to controls [12]. More recently, Suwa et al. [13] reported that CV in the interventricular septum was higher in patients who benefit from the beta-blocker therapy. Our results are consistent with previous observations in demonstrating a relatively large spectrum of cyclic MGL-variability in these patients. These results supported our hypothesis that this large spectrum of cyclic variability corresponds to the well-known variability of the natural history of this disease. In our group, CV indexes of septum and PW ranged from –2 to 26.4% and from –5.5 to 31%, respectively; and CV indexes of both septum and PW were severely depressed in patients with poor clinical outcome.

The underlying scenario to explain the relationship between depressed CV and poor prognosis can not be deduced from the results of our study. However, some other factors such as higher NYHA class and higher E/A ratio associating the depressed CV in patients with poor clinical outcome, suggests that depressed CV reflects the severity of IDC in a different manner. A discrepancy between wall thickening and CV has previously been reported in some pathological conditions such as stunned myocardium [22], and transplant rejection [23]. Therefore, the CV of tissue reflectivity appears to reflect intramural contractile performance rather than geometric phenomenon. Marini et al. showed that among the asynergic myocardial segments with comparable levels of wall thickness and wall motion score index those with relatively preserved CV index were viable [15]. These findings support the idea that CV of myocardial MGL reflects intramural contractile performance, and a more depressed CV could be a marker of more severely damaged myocardial tissue. In addition, PW–CV index was determined as the most significant independent prognostic indicator in our study group. This superiority of the index over conventional echocardiographic variables remains unclear. Previous studies conducted on larger number of patients with symptom status varying from class I to IV have defined the left ventricular systolic indexes and cavity diameters as the most powerful prognostic indicators [24,25]. However, in the subset of patients with more advanced heart failure symptoms, the EF may not correlate well with the prognosis [26]. The lack of prognostic value of left ventricular EF and cavity diameters in our study population may be explained by the highly symptomatic nature of our study group, which consisted of a relatively smaller number of patients.

4.1. Study limitations
The study population was small. Since videodensitometry requires a specific type of setting, no previously stored echocardiographic data could be used for textural assessment. Therefore, the number of patients was limited to those who were prospectively evaluated. An independent histological study would be of particular interest to elucidate the relation of depressed CV to disease severity, but we could not perform an additional simultaneous catheterization in the majority of cases and did not include this method in our study design. The quantitative myocardial texture analysis was performed using videodensitometry that might be influenced by native ultrasound signal modifications as a result of several processing steps in the echocardiographic instrument, mainly by the type of gray-level processing maps [27,28]. However, we believe that several potential sources of error were eliminated by adjusting the echocardiographic instrument to the same linear gray-level processing map in all patients and by using a parameter such as CV reflecting the relative changes of gray-level amplitude in the cardiac cycle rather than its absolute values. In addition, MGL have been corrected according to cavity gray levels in each patient. The effects of translation, rotation, and twist of the heart during cardiac systole as well as the anisotropic properties of myocardium may be the other factors influencing the results. In spite of these limitations, the videodensitometric method we used in this study is a relatively simple approach that can be widely applicable for myocardial texture analysis without requiring a sophisticated ultrasound system.

4.2. Conclusion
The severity of alteration in quantitative myocardial textural parameters is clinically relevant to patients with moderate to severe left ventricular dysfunction due to IDC. The assessment of severely depressed CV provides valuable prognostic information, which is relatively independent from the left ventricular cavity diameter and systolic functions in patients with IDC.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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