Early detection of myocardial dysfunction by echocardiographic
markers in patients with neuromuscular dystrophies
MARIO BURGOS, MARTA ROTELLA, SOFÍA BERMAN, GUSTAVO VÁZQUEZ PÁEZ, RODRIGO DE ROSA,
EDUARDO ESCUDERO, RICARDO RONDEROS.
Hospital de Clínicas Nicolás Avellaneda.
(4000) Tucumán, Argentina E-mail
Recibido 08-DIC-18 – ACEPTADO después de revisión el 27-ENERO-2018.
There are no conflicts of interest to disclose.
Duchenne (DMD) and Becker (BMD) muscular dystrophies affect the heart and sometimes with great clinical relevance. The aim of the study was to detect by echocardiographic markers that there is early myocardial dysfunction in patients with muscular dystrophies (MD). Methods: Case-control study, performed at the Nicolás Avellaneda Clinical Hospital in the city of San Miguel de Tucumán, Argentina, in the period between December 2012 and September 2013; with patients of the neurological rehabilitation service with diagnosis of Duchenne and Becker MDs. Echocardiographic markers values obtained were expressed as Average (A) and Standard deviation (SD), with 95% confidence intervals (CI 95). For the statistical analysis, Chi-square test and Fisher’s exact test were used. Results: Eighty-two patients were evaluated, 41 in the control group (CG) and 41 in the pathological group (PG) with MD. 83% of the patients had MD, 12% BMD and 5% DMD / BMD. There were statistically significant differences in the TEI index by TDI in the lateral, septal, and tricuspid walls and in the ejection period (p = 0.0001). There were also statistically significant differences in the TEI index of the mitral and tricuspid annulus with pulsed-wave Doppler (p = 0.0001), TAPSE and in the greater thickness of the RV free wall (p = 0.0001).
The ejection fraction (EF) in the PG had values within normal limits but lower than in the CG (63.9 ± 5% in PG vs 67.8 ± 2.6% in GC) (p = 0.0001). Conclusions: Markers of early myocardial dysfunction can be detected by two-dimensional echocardiography and pulsed-wave Doppler and TDI in patients with muscular dystrophies. Its routine use for diagnosis, monitoring, treatment, prognosis and evolutionary control is extremely useful. The screening method should include: EF, TEI index, pulsed and tissue Doppler, TAPSE and thickness of the RV free wall in cardiovascular evaluation.
Key words: Muscular dystrophies. Early myocardial dysfunction. Echocardiographic markers.
Muscular dystrophies (MDs) are a group of diseases that are characterized by neuromuscular tissue replacement by another one. Many of MDs affect the heart and occasionally with great clinical relevance, and may produce dilated or hypertrophic cardiomyopathy, as well as rhythm and electrical stimulus conduction disorders . Dystrophinopathies produce myocyte cellular hypertrophy, atrophy with necrosis, fibrosis with myocardial substitution by connective and fatty tissue .
In Duchenne muscular dystrophy (DMD) , dystrophin or regulation defects were found, with different degrees of cardiac dysfunction and skeletal muscle involvement. Skeletal muscle weakness, respiratory syndrome and electrocardiographic anomalies start at an early age, conditions correlated to different degrees of myocardial compromise.
Becker muscular dystrophy (BMD) is an inherited disorder linked to X chromosome, characterized by progressive muscle weakness, infrequent in young people, but with a possible myocardial involvement , with this involvement not advancing as in DMD .
Cardiac compromise is present in approximately 90% of Duchenne and Becker dystrophies, but is a cause of death in approximately 20% of DMD cases and 50% of BMD cases [5,6].
Doppler echocardiography (DE) is the gold standard for the evaluation of systolic function, by ejection fraction (EF). It is possible to verify LV dilatation, diffuse hypokinesis, decreased EF, mitral valve flow pattern of prolonged relaxation, mitral insufficiency, etc. To be able to detect and diagnose the early impairment of cardiac function have proven to be useful: myocardial performance (TEI) index , pulsed-waved Doppler echocardiography  and tissue Doppler imaging (TDI) allow to detect early changes in systolic and diastolic cardiac function , not requiring a good resolution in 2D echo, providing specific information about myocardial tissue velocities and tension.
To detect early myocardial dysfunction (EMD) by echocardiographic markers in patients with MD.
To describe parameters of ventricular function applying Doppler echo in patients with DM indicating EMD and to compare them to the control group (CG).
To determine EMD markers and relate them to the degree of neuromuscular compromise with the use of cardiac Doppler echo.
To relate echocardiographic and electrocardiographic parameters on the occasion of heart involvement in the population studied.
To relate in patients with MD, electrocardiographic parameters with the Vignos scale.
MATERIALS AND METHODS Case-control study: Performed at the Nicolás Avellaneda Hospital, in San Miguel de Tucumán, Argentina, from December 2012 to September 2013.
Inclusion criteria: Patients from the neurological rehabilitation service with diagnosis of muscular dystrophies (MDs) constituted the pathological group (PG). (Figure 1)
Figure 1. Distribution of patients with muscular dystrophies (n=41).
Exclusion criteria: All other MD that were not mentioned above, patients with cardiovascular diseases, diabetes and hypertension, as these conditions may alter electrocardiographic and echocardiographic patterns.
The CG was constituted by patients with no diagnosis of MD.
Echocardiographic parameters (LVEF, TEI index, ejection period [EP], isovolumic relaxation [IVR]) in the studied population, both in the left and the right ventricles , were evaluated by transthoracic, M mode, 2D, Doppler (pulse-waved, continuous-wave, tissue and color) echocardiography, according to standardized protocols , using acoustic windows and conventional views (parasternal long axis, parasternal short axis, apical 2, 3, 4 and 5 chambers (Figure 2), subcostal and suprasternal), occasionally adding nonconventional windows.
Figure 2. Echocardiogram of a young, 16-year-old man with DMD.
Apical 4-chamber view and evaluation by TDI at the level of the lateral wall of the mitral annulus.
The echocardiography device software of the institution was used, Esaote Mylab 50. Static images and video clips were stored in a digital format in the hard disk of the device to enable the possible repetition of the measurements with the same software.
The electrocardiograph used to make 12-lead recordings was a Cardiotecnica RG501 device, of one channel, with which the following were assessed: heart rate, the presence of high R waves, Q waves in DI and early detection of the characteristics proper of MD, sinus tachycardia in rest, >100 beats per minute, R waves >10 mm or 0.10 mv in precordial leads from V1 through V6, and Q waves in DI, aVL, V5-V6 (Figure 3).
Figure 3. Electrocardiogram showing the characteristics proper of DMD that include: tachycardia in rest with heart rate close to 90 bpm, increase of R waves width in precordial leads V1, V2 and V3; and Q waves in lateral and inferior leads (II, III, aVF, V4, V5, V6).
Figure 4. Echocardiographic findings and Vignos scale (n=41), according to the degree of neuromuscular impairment: minimum 1; mild 2 to 4; moderate 5 to 7; severe 8.
To detect early myocardial dysfunction (EMD), echocardiographic values were compared in the CG to those of the PG, and the existence of EMD was considered to exist in those presenting statistically significant differences in regard to normal values according to the degree of neuromuscular impairment.
The stage/degree of impairment of MD was evaluated by the Vignos scale , which is used in the rehabilitation service of the hospital (Table 1). Least compromise was scored as 1, most compromise as 10, and the minimum impairment stage was classified as 1, mild impairment 2 to 4, moderate 5 to 7, and severe 8 to 10.
Table 1. Vignos scale. Score according to muscular dystrophy compromise.
Neuromuscular impairment: minimum 1; mild 2 to 4; moderate 5 to 7; severe 8.
Neuromuscular compromise / Vignos scale
The patient walks and climbs stairs, not requiring help.
The patient walks and climbs stairs, with the help of a handrail.
The patient walks and climbs stairs slowly, with the help of a handrail.
The patient walks, not requiring help, and can sit up, but cannot climb stairs.
The patient walks, not requiring help, but cannot sit up or climb stairs.
The patient walks alone with help, or walks independently with the help of a long leg orthopedic device
The patient walks with the help of a long leg orthopedic device, but requires help to keep the balance.
The patient stands with the help of a long leg orthopedic device, but is unable to walk, even with help.
The patient is in a wheelchair, and is able to bend elbows against gravity.
The patient is in a wheelchair or in a bed, and cannot bend elbows against gravity.
Statistical analysis: The evaluation of the results of the parameters obtained from the pathological group patients was made by comparing them to the normal values indexed by body surface according to the values reported by the American Society of Echocardiography (ASE). They were expressed as average (A) and standard deviation (SD) with confidence intervals of 95% (CI 95). Chi-squared test and Fisher’s exact test were applied to the evaluation of relationships between echocardiographic and electrocardiographic parameters, and for the electrocardiographic parameters relationships, the Vignos scale was applied.
Ethical considerations: The patients signed an informed consent of confidentiality, guaranteeing the data gathered would be exclusively used by the investigator.
There were 82 patients evaluated (41 in the CG and 41 in the PG). The mentioned groups were homogeneous in the demographic characteristics of the population studied, with no statistical difference in age (CG 14.5±7.8 years vs PG 12.7±5.9) (p=0.24).
Figure 1 shows the distribution of the types of muscular dystrophies in the population studied in the pathological group.
When comparing the CG and the PG, there were statistically significant differences in the assessment of different myocardial function markers.
Ejection fraction (EF): the PG presented EF values within normal limits, but lower than in the CG (63.9±5% PG vs 67.8±2.6%) (p=0.0001).
Pulsed-wave Doppler (PWD) in the mitral annulus: the TEI index in the CG was 0.3±0.1 vs 0.4±0.1 in the PG (p=0.0001); the ejection period (EP) in the CG was 255.4±29.6 milliseconds (ms) vs 238.2±29.2 (ms) in the PG (p=0.009).
Lateral wall TDI: it showed only a difference in the highest value of the TEI index, in the CG 0.4±0.1 vs 0.5±0.1 in the PG (p=0.0001). (Figure 2).
Septal TDI: it was found that the isovolumic relaxation (IVR) time in the CG was 54.5±12.0 ms vs 63.5±8 ms in the PG (p=0.001); the TEI index (in the CG 0.4±0.1 vs 0.6±0.7 PG) (p=0.07) and the ejection period (EP) in the CG 274.6±32.2 ms vs 226.5±23.6 ms of the PG (p=0.0001).
Tricuspid annulus PWD: there were significant statistical differences in the TEI, which in the CG was 0.3±0.1 vs PG 0.4±0.2 (p=0.005).
Tricuspid annulus TDI: it was found that IVR in the CG was 55.2±16.9 vs 65.4±15 in the PG (p=0.005); the TEI index was in the CG 0.4±0.1 vs 0.6±0.1 in the PG (p=0.0001); and EP in the CG was 264.7±46.9 ms vs 210±37.1 ms in the PG (p=0.0001).
In the assessment of the right ventricle (RV), the PG presented less TAPSE (tricuspid annular plane systolic excursion) than the CG, with a statistically significant difference (p=0.0004).
Right ventricular free wall thickness: the PG presented more thickness than the CG, a statistically significant difference (p=0.00001).
Comparison between the echocardiographic findings and the Vignos scale on clinical compromise.
When considering the stage of neuromuscular impairment by the Vignos scale (Table 1) in the PG, 37% presented a moderate compromise with a score of 5 to 7 (15 out of 41 patients), 34% had a severe compromise with a score of 8 to 10 (14 out of 41 patients); 22% presented a mild compromise with a score of 2 to 4 (9 out of 41 patients) and finally 7% had a minimum compromise with a score of 1 (3 patients).
In those that had severe neuromuscular impairment (Vignos score 8 to 10) there were statistically significant differences, in the ejection period (EP) and the lateral and septal walls and tricuspid ring TDI, as shown in Table 2.
Table 2. Comparison between the echocardiographic findings and the Vignos scale on compromise (n=41)
wall by TDI
Tricuspid annulus TDI
Stage IV vs no compromise: EP lateral wall TDI: p=0.001 / Stage IV vs no compromise: septal TDI: p=0.002 / Stage IV vs no compromise: tricuspid annulus: p=0.001.
In the search for the strength of the association between early myocardial dysfunction (EMD) (echocardiographic and electrocardiographic), there was significant statistical association between: R wave: with the TEI index by pulsed-wave Doppler (PWD) of the mitral annulus (p=0.001), with the TEI index by TDI of the lateral wall (p=0.00001), with the TEI index by septal TDI (p=0.001) and RV free wall thickness (p=0.0001). Q wave in DI: with the TEI index by PWD of the mitral annulus (p=0.002); with TEI index by TDI of lateral wall (p=0.0001) and RV free wall thickness (p=0.00001). Q waves in aVL: with the TEI index by PWD of the mitral annulus (p=0.002), with TEI index by TDI of lateral wall (p=0.0003) and RV free wall thickness (p=0.00001). Q waves in V5-V6: with the TEI by PWD of mitral annulus (p=0.0005), with TEI index by TDI of lateral wall (p=0.00001), with TEI index by septal TDI (p=0.003) and RV free wall thickness (p=0.00001).
When relating the electrocardiographic parameters of early myocardial dysfunction (high R waves in precordial leads and Q waves in DI-aVL-V5-V6)  with the Vignos scale, in the population in study it was found that 100% of patients with PG presented abnormal ECG, regardless of the degree of neuromuscular impairment.
Echocardiogram is a tool, which due to costs and information that it may provide, it is extremely useful for diagnosis and for the degree of development of cardiomyopathy in patients with DMD.
Until recently, in children with DMD, survival did not exceed 15 to 20 years due to added respiratory and cardiac complications (congestive heart failure or arrhythmias), but currently many of these patients with DMD exceed the abovementioned survival limit .
A greater longevity has led to the assessment of heart function and cardiovascular health being an increasingly significant aspect of the evaluation and treatment of Duchenne muscular dystrophy.
The American Academy of Pediatrics  has pointed out that the time for the development of cardiomyopathy has not been characterized, as neither the relevant diagnostic tests to study cardiac dysfunction in DMD or BMD carriers, so it is recommended to optimize the diagnostic tests for an early detection of myocardial dysfunction.
The early diagnosis of LV function impairment, by providing information about the initial stage of myocardial dysfunction may partially improve the prognosis of this disease, as treatment starts in a subclinical stage of the disease .
It is important to remember that the classical symptoms and signs of heart failure once they manifest clinically, do not entail an early, but an advanced myocardial compromise.
Echocardiography is the most universally standardized method for the evaluation of cardiac function. Preserving EF within normal limits in patients with MD and the absence of changes in the classical echocardiographic measurements in the evaluation of both ventricles, both in systole and diastole, manifest the significance of resourcing to other techniques such as using tissue Doppler imaging (TDI) and myocardial function index (TEI), to detect early myocardial dysfunction (EMD).
The estimation of the TEI index is feasible in DMD and it allows to detect anomalies in this parameter in 80% of patients; while EF was abnormal only in 40% of these patients.
The TEI index is easy to obtain using Doppler images and it has shown to be, in animal models, closely related to EF . Useful for an early detection of concealed cardiac dysfunction in patients with DMD when other simple and standard echocardiographic parameters are within normal limits .
In cardiomyopathies by dystrophin , tissue Doppler imaging (TDI) is a useful tool to evaluate diastolic dysfunction , and for an early identification of regional systolic alterations in patients carriers of normal EF in presymptomatic patients carriers of inherited cardiomyopathies of genetic and molecular basis . TDI has become a supplementary tool for conventional diagnostic evaluations with electrocardiogram and echocardiography, as part of the screening for an early diagnosis of cardiomyopathy.
In the case of BMD, as previously stated, there is less myocardial damage than in the patients with DMD; nevertheless, heart failure is more frequent as the cause of death in this muscular dystrophy .
Using TDI with its improvements perfected and provided accuracy, undoubtedly, for the early identification of structural abnormalities and jointly with this, for the diagnosis of these inherited cardiomyopathies ; besides enabling a longitudinal follow-up of these patients.
In young patients with DMD that have normal overall systolic function, reductions in the parameters of systolic deformation, as well as a reduction in the first diastolic myocardial velocities can be detected in the LV antero-lateral and infero-lateral walls .
In this study, the statistically significant differences in the EF values between both values (PG vs CG) may indicate that muscular dystrophy (MD) affects LV systolic function, with its values not being below parameters considered normal, in the early stages of the disease, in such a way that prospective, follow-up studies will be necessary to assess this finding.
Right ventricular function impairment (TAPSE) would require more evaluations to establish its relationship to the disease; in spite of the right ventricle apparently being normal in size and with a preserved function.
Increases in the TEI index of the mitral annulus by PWD and TDI, in the presence of a smaller value of ejection period, could be an indication that the difference in the TEI index does not occur at the expense of the ejection period, but of the rest of its components. The estimation of the TEI index, feasible in DMD, detected anomalies in this parameter in 79% of patients, while EF was abnormal only in 40% of the studied population.
Evaluating cardiovascular health in this particular group of patients is closely related to the chance of properly using and interpreting new ultrasound techniques for an early diagnosis of cardiac function impairment in echocardiographically “normal” hearts, which in fact are not so normal, which may lead to modifications in the evolution and survival of patients carriers of muscular dystrophies.
Electrocardiographic evaluation provides valuable information as a negative predictive marker of myocardial fibrosis with a pretty accurate echocardiographic correlation . Patients presenting with ECG anomalies had a strong association with multiple echocardiographic parameters of dysfunction in both ventricles.
When linking different electrocardiographic parameters to the Vignos scale, ECG anomalies were present in all patients with MD; even in those patients with lowest score in this scale; a very significant datum for an early electrocardiographic assessment of myocardial dysfunction.
The new techniques for an early diagnosis of myocardial dysfunction, as in the case of speckle tracking echocardiography (STE), turned out to be useful to detect early regional myocardial dysfunction. The velocity of myocardial deformation by STE is useful to detect diastolic cardiac function impairment in DMD, with no obvious LV dilatation or the presence of clinical signs. Also, the velocity of radial deformation of ventricular chambers could be useful to detect an early deterioration of the myocardium in DMD .
Another useful tool for the evaluation of MD is cardiac magnetic resonance imaging (MRI) used mainly in the assessment of patients with DMD; providing noninvasive, reliable and sensitive measurements of cardiac function .
By Tagging, it is possible to obtain additional information about myocardial impairment, another early potential marker of myocardial dysfunction, which along late gadolinium enhancement allows to identify fibrosis areas of the middle and subepicardial walls in patients with MD .
The physical characteristics of patients with DMD that include, among others, barrel chest, increase in chest wall fat, scoliosis and the position they adopt, may make the performance of echocardiographic tests more difficult and complicated in them.
Multi and interdisciplinary assistance (neurologists, orthopedic surgeons, physiatrists, etc.) that is required by patients carriers of MD occasionally makes the chance to assess early cardiological function difficult, with a real impact on cardiovascular morbidity and mortality for this population.
The size of the sample to draw conclusions is also a significant limitation, which should be taken into account.
According to the findings of this study, it would be advisable for echocardiographic markers of early myocardial dysfunction (2D and Doppler): EF, TEI index, PWD and TDI (lateral, septal and tricuspid walls), EP, TAPSE and RV free wall thickness increase to be added as a screening method in the cardiovascular evaluation of neuromuscular dystrophies.
We should also highlight that there are electrocardiographic markers (high R waves in precordial leads and Q waves in DI-aVL-V5-V6) that are extremely valuable to take into account for the diagnosis of early myocardial dysfunction, with an accurate echocardiographic correlation.
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