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European Journal of Echocardiography 2005 6(4):243-250; doi:10.1016/j.euje.2004.09.010
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Copyright © 2004, The European Society of Cardiology

The use of Tissue Doppler Imaging for the assessment of changes in myocardial structure and function in inherited cardiomyopathies

J. De Backera,b,*, D. Matthysc, T.C. Gilleberta, A. De Paepeb and J. De Suttera

aDepartment of Cardiovascular Medicine, University Hospital, Ghent, Belgium
bDepartment of Medical Genetics, University Hospital, De Pintelaan 185, 9000 Gent, Belgium
cDepartment of Pediatrics, University Hospital, Ghent, Belgium

Received 29 June 2004; received in revised form 20 September 2004; accepted after revision 22 September 2004.

* Corresponding author. Tel.: +32 9 240 36 03; fax: +32 9 240 49 70. E-mail: julie.debacker@ugent.be


   Abstract
Top
 Abstract
Introduction
 Tissue Doppler Imaging (TDI)
 Inheritable disorders examined...
 Discussion
 References
 
Although there is still a long way to go, our understanding of the genetic basis of cardiomyopathies – dilated or hypertrophic – has significantly improved over the past decade. This new and intriguing era of cardiogenetics has already answered some important questions concerning the pathophysiology of these disorders, but it has also raised some new questions: how do we define "presymptomatic" mutation carriers? Should we treat them? Do we have any diagnostic tools to identify the presymptomatic subjects in those families where the underlying mutation has not been identified yet?

To address at least part of these questions, there is a clear need for screening techniques in the early stage of the disease which have to be sensitive and non-invasive.

In recent years Tissue Doppler Imaging (TDI) has emerged as a well suited technique for these purposes and several interesting papers on this issue have been published.

This paper reviews the findings from TDI in several forms of inherited cardiomyopathy. Although the implementation of this technique in everyday clinical practice still requires some refinement, the results from these studies are encouraging and TDI is likely to be complementary to other established screening tools such as ECG and conventional echocardiography.

Keywords: Cardiomyopathy; Tissue Doppler Imaging; Genetic


   Introduction
Top
 Abstract
 Introduction
Tissue Doppler Imaging (TDI)
 Inheritable disorders examined...
 Discussion
 References
 
In the past decade, many disease-causing genes have been identified for several cardiovascular disorders. This is especially the case for different variants of cardiomyopathy.

However, the onset of clinical symptoms in many of these diseases is highly variable. At present, management options in mutation carriers, free of symptoms are not clearly established. Identifying myocardial involvement before the appearance of obvious clinical symptoms is important, both for therapeutical purposes and for counseling in these patients and their families. Therefore, more accurate diagnostic investigations are needed to identify persons at risk in an early stage of the disease. As these investigations have to be performed on asymptomatic subjects, they have to be non-invasive, highly sensitive and specific.

In recent years Tissue Doppler Imaging (TDI) has emerged as a technique for the detection of structural abnormalities in the myocardium. Several inheritable disorders with cardiac involvement have been examined with TDI.

In this brief overview, we will summarize these findings.


   Tissue Doppler Imaging (TDI)
Top
 Abstract
 Introduction
 Tissue Doppler Imaging (TDI)
Inheritable disorders examined...
 Discussion
 References
 
TDI is a relatively new echocardiographic technique which is applicable for the quantification of myocardial velocities.1,2 It can be used to assess global and regional systolic left ventricular (LV) function and to identify abnormal LV relaxation in a variety of conditions. TDI requires modifications in signal processing of the returned Doppler signals. As tissue velocities are typically much lower than the conventional velocities of blood flow (–30 to +30cm/s versus –200 to +200cm/s), both filter adjustment and gain amplification are necessary. TDI can be used to measure tissue velocities in different segments of the myocardium, both in systole and in diastole. This gives us information about the regional segmental myocardial function. Moreover, TDI can also be applied for measurement of velocities at different sites of the mitral valve annulus (anteroseptal, lateral, inferior, anterior, posterior and inferoseptal). These latter velocities reflect the longitudinal vector of shortening and lengthening of myocardial segments. This provides an appreciation of the ventricular function along the longitudinal axis. Wall motion in the radial direction may be assessed as well from parasternal views. This analysis allows evaluation of a myocardial velocity gradient between subendocardium and subepicardium. A decrease of this gradient appears to be a promising tool for detecting subtle, subclinical systolic myocardial dysfunction.3 Besides its applications to quantify systolic and diastolic hemodynamic events, TDI has the advantage that it allows to sample regional and segmental myocardial areas and to perform quantitative analysis of the intramyocardial velocity profiles across the walls.

Essentially, 2 different modalities of TDI are available: color TDI and Pulsed Wave (PW) TDI. Each technique has its own advantages and disadvantages.

Color TDI is visually appealing and easily discloses differential velocities between the subendocardial and subepicardial layers during systole and diastole. With color TDI, a higher velocity of shortening and relaxation can be observed in the endocardium compared with the epicardium, and it can be quantified as a myocardial velocity gradient (MVG). Pulsed TDI, as opposed to color TDI, offers improved temporal resolution and the ability to quantify peak rather than mean myocardial velocities. It does not require off-line analysis, and it provides instantaneous display of the Doppler spectral information. Fig. 1 illustrates pulsed TDI (A) and color TDI (B) recordings in a patient and a control with hypertrophic cardiomyopathy.


Figure 1
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  		Figure 1 Illustration of pulsed TDI (A) and color TDI (B) recordings in a patient with HCMP (upper panel) and an aged matched normal control (lower panel). Note the differences in the velocity scale between the patient and the control. Sa: peak systolic velocity at the septal mitral annulus. Ea: peak early diastolic velocity at the septal mitral annulus. Aa: peak late diastolic velocity at the septal mitral annulus.

 
The nomenclature in TDI is somewhat confusing, with different notations for the same measurement across the literature. We tried to unify the different notations and we will use the following abbreviations:
Em: peak early diastolic velocity in the myocardium,
Am: peak late diastolic velocity in the myocardium,
Sm: peak systolic velocity in the myocardium,
Ea: peak early diastolic velocity at the mitral valve annulus,
Aa: peak late diastolic velocity at the mitral valve annulus,
Sa: peak systolic velocity at the mitral valve annulus.


   Inheritable disorders examined with TDI
Top
 Abstract
 Introduction
 Tissue Doppler Imaging (TDI)
 Inheritable disorders examined...
Discussion
 References
 
Hypertrophic cardiomyopathy
Hypertrophic cardiomyopathy (HCM) is an autosomal dominant disorder characterized by left ventricular hypertrophy (LVH), abnormalities of diastolic function and increased risk of sudden death. HCM affects 1 in 500 persons according to echocardiographic criteria.4 To date, 10 different genes encoding components of the sarcomere have been implicated in HCM.5

The presence or absence of LVH is not an infallible diagnostic criterion and the spectrum of hypertrophy is broad, even among individuals with the same mutation.6 Furthermore, because full expression of the HCM phenotype typically does not occur until adolescence or thereafter, establishing the clinical diagnosis of HCM early in life may be particularly challenging. An alternative approach to a preclinical diagnosis of HCM is genetic testing, which could identify mutation positives independently of and before the development of LVH. However, genetic testing still has some major drawbacks: the presence of substantial genetic heterogeneity, the presence of multiple mutations within the same gene and the presence of yet unidentified genes. Furthermore, the type of mutation does not appear to have any prognostic value.7

Myocardial contraction and relaxation abnormalities, detected with pulsed TDI have been demonstrated in a transgenic rabbit model of human hypertrophic cardiomyopathy.8 These results were confirmed in several human studies, comparing normal controls to patients with an identified mutation, with or without left ventricular hypertrophy (M+/LVH+ and M+/LVH–, respectively). The results from these studies are summarized in Table 1. Both systolic and diastolic velocities at the mitral annulus and at the myocardium appear to be reduced in HCM patients, irrespective of the presence of LVH. Conventional echocardiographic parameters of systolic and diastolic function showed no significant differences. These reduced TD velocities were present consistently for a variety of mutations in β myosin heavy chain, cardiac troponin T, and myosin binding protein C.9 It has to be emphasized that despite the presence of statistically significant differences between patients and normal subjects, substantial overlap is present. Adding additional parameters such as left ventricular ejection fraction increased the predictive value in one study.10


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  		Table 1 Pulsed TDI in hypertrophic cardiomyopathy

 
Evolutionary changes in mutation carriers have also been assessed in a small study, showing a significant inverse relationship between the extent of hypertrophy and severity of baseline dysfunction by TDI.11

Friedreich's ataxia (FRDA)
FRDA is an inherited neurodegenerative disorder associated with cardiomyopathy and impaired glucose tolerance. The genetic basis for FRDA is a GAA trinucleotide repeat expansion in the first intron of gene X25, which encodes for the protein Frataxin. The most common echocardiographic abnormality is asymmetrical LV hypertrophy and thickening of the papillary muscles, although the range of abnormalities appears to be wide.

Dutka et al. demonstrated with TDI that Myocardial Velocity Gradients (MVG) in systole and during rapid ventricular filling phase of early diastole are reduced in patients with FRDA who are without cardiac symptoms12 (Table 2).


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  		Table 2 TDI in Friedreich's ataxia

 
Age corrected MVGs were inversely related to the size of the GAA triple repeat expansion in all phases of the cardiac cycle. They hypothesize that the abnormal MVG reflects the decreased myocardial contractility and relaxation secondary to abnormal mitochondrial function resulting from reduced levels of Frataxin in FRDA.

Myotonic dystrophy (Steinert's Disease)
Myotonic dystrophy (DM) is a multisystem disorder that affects skeletal muscle and smooth muscle, as well as the eye, heart, endocrine system, and central nervous system. It's prevalence is estimated at 1/20,000.13

DM is inherited in an autosomal dominant manner. Diagnosis is confirmed by detection of an expansion of the CTG trinucleotide repeat in the DMPK gene (chromosomal locus 19q13.2-q13.3). Cardiac conduction defects of varying degrees of severity are common, up to 90% in one series.14 Less commonly, cardiomyopathy may occur.13

Fung et al.15 conducted a prospective trial in 22 patients with DM without known heart failure to assess whether there is subclinical impairment of LV contractility using conventional 2D echocardiography and TDI. LV ejection fraction did not differ between the patient group and the controls. Sm at the basal lateral and basal septal segments as well as lateral Sa velocities were significantly lower in subjects with DM when compared to controls (Table 3). Furthermore, peak systolic velocities correlated inversely with neurologic severity. There was no correlation with the trinucleotide repeat length. There were no significant differences in the diastolic parameters (both with conventional echocardiography and with TDI).


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  		Table 3 Color TDI in myotonic dystrophy

 
Becker muscular dystrophy
Becker Muscular Dystrophy (BMD) is an X-linked recessive muscular disease characterized by progressive muscular weakness and cardiac involvement caused by dystrophin abnormalities in all striated muscles as well as in the myocardium. The prevalence is estimated at 2.38/100,000.16 Eventually patients as well as female carriers will develop a dilated cardiomyopathy. Both in BMD patients and in female carriers myocardial damage can be detected in a preclinical stage through minor electrocardiographic and echocardiographic signs.

Agretto et al. have shown that most of the regional pulsed TDI diastolic indices were decreased in BMD patients and carriers, when compared to normal subjects17 (Table 4). Besides confirming systolic alterations of BMD patients with reduced LVEF, pulsed TDI had detected early segmental systolic abnormalities in BMD patients with normal LVEF and in female carriers. These results support the hypothesis that TDI may represent an independent marker of early systolic dysfunction compared to standard echocardiography.


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  		Table 4 Pulsed TDI in Becker muscular dystrophy

 
Gamma-sarcoglycanopathy
Gamma-sarcoglycanopathy, also classified as limb girdle muscular dystrophy type 2C (LGMD2C), is due to mutations in 13q12 and subsequent gamma-sarcoglycan deficiency. This protein is one of the components of the so-called dystrophin associated glycoprotein (DAG) complex which links dystrophin and possibly other cytoskeletal muscle proteins to the extracellular matrix. The inheritance is autosomal recessive and patients of both sexes are equally affected. Cardiac involvement is frequent in dystrophinopathies and at least one of the pathogenetic mechanisms is thought to be related to the lack or paucity of dystrophin in cardiac muscle fibers, parallel to dystrophin deficiency in skeletal muscle fibers.

Calvo et al. analysed mitral and tricuspid annular velocities with pulsed wave TDI in 10 children free of clinical cardiovascular disease.18 Ea was higher in patients than in controls. At tricuspid annulus level, patients exhibited lower Sa and higher Aa velocity values (Table 5). This study shows that subclinical myocardial dysfunction in patients with Gamma-sarcoglycanopathy can be demonstrated with TDI.


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  		Table 5 Pulsed TDI velocities in patients with gamma-sarcoglycanopathy

 
Fabry disease
Fabry disease is an X-linked disorder caused by a deficiency of lysosomal enzyme {alpha}-galactosidase A. The disorder is caused by mutations in the {alpha}-Gal A gene located in the X chromosomal region Xq22. The incidence is estimated at ~1 in 50,000 males.19 Cardiac involvement is very common and is the most important cause of death in affected patients.20 Moreover, the heart can be the only organ involved in female carriers21 and in male patients with specific gene mutations, the so-called "cardiac Fabry variant". The cardiac involvement is characterized by progressive severe left ventricular hypertrophy that mimics an obstructive or non-obstructive hypertrophic cardiomyopathy.22

Detection in a preclinical stage of the disease is important with respect to treatment with an enzyme replacement therapy. When this can be administered in an early stage, early complications like electrical instability and thromboembolic events can be avoided.23 Conventional non-invasive tools such as ECG, 2D-echocardiography and even MRI are unable to identify the preclinical phase of Fabry cardiomyopathy.24

A study comparing 20 patients (10 M+/LVH+, 10 M+/LVH) to 10 healthy control subjects demonstrated that all mutation positive patients had significantly reduced Sa, Ea and Aa velocities at both corners of the mitral annulus when compared to normal subjects (Table 6). Thus, TDI can provide a preclinical diagnosis of Fabry cardiomyopathy, allowing early institution of enzyme replacement therapy.


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  		Table 6 Pulsed TDI in Fabry disease

 

   Discussion
Top
 Abstract
 Introduction
 Tissue Doppler Imaging (TDI)
 Inheritable disorders examined...
 Discussion
References
 
Fifty years ago, Watson and Crick published their famous article "Molecular structure of Nucleic acids: a structure for Deoxyribose Nucleic Acid".25 Since then, innumerable genetic disorders have been identified. This has lead to a better understanding of the pathophysiology of many disorders. Furthermore, genetic screening has significant impact on early identification, risk stratification and implementation of measures to prevent or attenuate evolving phenotype. Expectations are very high for the applications of molecular genetics in daily clinical practice – both among the public and among the clinicians. For many diseases, however, molecular genetic screening has been hampered by factors such as the diversity of known genes and mutations as well as by the presence of yet-to-be-identified genes.

Dealing with genetic disorders demands major changes in the way we think about a "disease". One should get familiar with terms like "mutation carrier" and "presymptomatic testing". The distinction between a pure presymptomatic state and the occurrence of the first signs of the disorder may be very subtle. This is however important, especially in cardiovascular diseases, where life threatening events should be prevented in as many cases as possible.

An indirect and yet promising outcome of the genetic studies of cardiomyopathies has been the use of Tissue Doppler Imaging for an early identification of mutation carriers. Indeed, Tissue Doppler echocardiography may be helpful in increasing our understanding of the changes in myocardial structure and function in inherited cardiomyopathies. The different findings are summarized in Table 7.


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  		Table 7 Overview of the different inherited cardiomyopathies studied with TDI

 
Nevertheless, TDI application in these disorders has some major limitations: as can be appreciated from the figures listed in the different publications, the variability in the measurements obtained with TDI is substantial. This is particularly so for the myocardial tissue velocities and to a lesser extent for the mitral annular velocities. There are several explanations for this variability.

First, the number of patients included in each study is small; increasing the amount of subjects studied will reduce the standard deviation obtained for each measurement. Second, while comparing the results from different studies for clinical use, it is important to carefully match for age, as TDI velocities are highly age dependent. Diastolic velocities decrease more with age than do systolic velocities.26,27 A third possible explanation for the wide range in values obtained with TDI might be due to different settings between different echo machines. Another important issue concerning the use of TDI in these disorders is that it has no diagnostic value, it is not specific for any disorder. Reduced TDI velocities indicate segmental dysfunction which may be related to a specific clinical condition.

In summary, these limitations emphasize the need for uniformisation of the obtained normal values throughout the literature. This will only be possible by means of large-scale (multicentre) trials in a study group with a wide age range.

In spite of these limitations, we still believe that TDI, along with other established screening tools like conventional echocardiography and ECG, might play a complementary role in genetic screening of patients and family members with different kinds of cardiomyopathy. In selected cases, such as Fabry disease, TDI could be helpful to identify patients who could benefit from therapy with enzyme replacement. Experimental data in transgenic animals have shown the reversibility of the histological phenotypes in HCM through early angiotensin II blockade.28 TDI could be a valuable tool to select those patients considered to derive benefit from such a treatment.


   References
Top
 Abstract
 Introduction
 Tissue Doppler Imaging (TDI)
 Inheritable disorders examined...
 Discussion
 References
 

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Technological advances in tissue Doppler imaging echocardiography
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