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 Table of Contents  
Year : 2019  |  Volume : 17  |  Issue : 4  |  Page : 409-416

Early detection of left ventricular involvement in patients with Duchenne’s and Becker’s muscular dystrophy

1 Department of Cardiology, Faculty of Medicine (for Girls), Al-Azhar University, Cairo, Egypt
2 Department of Neurology, Faculty of Medicine, Al-Azhar University, Cairo, Egypt

Date of Submission17-Jul-2019
Date of Decision16-Sep-2019
Date of Acceptance14-Oct-2019
Date of Web Publication14-Feb-2020

Correspondence Address:
Shaimaa A Habib
Department of Cardiology, Faculty of Medicine (for Girls), Al-Azhar University, Cairo, 11827
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/AZMJ.AZMJ_95_19

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Background Patients with Duchenne muscular dystrophy (DMD) and Becker’s muscular dystrophy (BMD) may have asymptomatic cardiac involvement for years before the development of dilated cardiomyopathy and even showed normal conventional echocardiographic parameters. We evaluated those patients with more recent echo modalities for early detection of subtle cardiac changes.
Patients and methods Thirty patients [13 with BMD as group 1 (G1) and 17 with DMD as group 2 (G2)] compared with 30 age-matched and sex-matched healthy participants as group 3 (G3). All cases were subjected to history taking, clinical examination, ECG, conventional two-dimensional (2D) echocardiography, tissue Doppler imaging, 2D-speckle tracking echocardiography, and 4D echocardiography for measurement of left ventricular (LV) dimensions, systolic and diastolic function with focus on strain imaging modality.
Results Nine patients of G2 and three patients in G1 had LV systolic dysfunction despite normal 2D-LV ejection fraction. Ten patients in G2 and five patients in G1 had LV diastolic dysfunction measured by LV early diastolic wave velocity over mitral valve measured by conventional Doppler/early diastolic mitral annular velocity by tissue Doppler imaging (E/Ea). Tissue Doppler myocardial performance index was significantly higher in both G1 and G2. 2D-LV septal strain, lateral strain, anteroseptal, 2D-global longitudinal strain (GLS), and 4D-GLS strains were significantly lower in G1 and G2. Apical, mid, and basal posterior LV strain were significantly lower in G2 compared with G1. 2D-GLS was lower in G2 compared with G1. Both LV global radial strain and global circumferential strain were significantly lower in G1 and G2. Mid and basal septal strain and basal posterior strain were significantly lower in G2 compared with G1. The mid and basal posterior strains were significantly lower in G2 compared with G1.
Conclusion 2D-speckle tracking and 4D echocardiographic study of global and regional strain besides creatinine phosphokinase serum levels may add benefit in early detection of subtle LV dysfunction in patients with DMD and BMD.

Keywords: two-dimensional-speckle tracking echocardiography, four-dimensional-echocardiography, becker muscular dystrophy, cardiomyopathy, duchenne

How to cite this article:
Habib SA, Mohamed MT. Early detection of left ventricular involvement in patients with Duchenne’s and Becker’s muscular dystrophy. Al-Azhar Assiut Med J 2019;17:409-16

How to cite this URL:
Habib SA, Mohamed MT. Early detection of left ventricular involvement in patients with Duchenne’s and Becker’s muscular dystrophy. Al-Azhar Assiut Med J [serial online] 2019 [cited 2020 Jul 6];17:409-16. Available from: http://www.azmj.eg.net/text.asp?2019/17/4/409/278407

  Introduction Top

Muscular dystrophies are a group of hereditary muscle disorders characterized by progressive wasting and weakness with variable age of onset, distribution, and severity [1].

Duchenne muscular dystrophy (DMD) and Becker muscular dystrophy (BMD) are allelic X-linked types of neuromuscular diseases. Worldwide, prevalence of DMD and BMD has ranged from 0.1 to 1.8 per 10 000 male individuals with higher rate in DMD [2].

Cardiac involvement varies from asymptomatic ECG changes to conduction disorders requiring pacing or end-stage dilated cardiomyopathy which is progressive and associated with left ventricular (LV) failure, ventricular arrhythmias, and is an important cause of morbidity and mortality in those patients [3].

Boys with DMD can have rapid progression of LV dysfunction without symptoms necessitating accurate and careful evaluation of cardiac function. Thus, initial cardiac evaluation should be starting at 6 years of age biannually till the age of 10 years, then annually with closer evaluations if cardiac imaging abnormalities appeared [4].

Echocardiography is a feasible and easy way to examine the heart; however, it may show normal left ventricular ejection fraction (LVEF). So, EF may not be a suitable parameter to detect asymptomatic cardiac involvement [5].

On that basis we tried to evaluate the LV function and structure using more recent echo modalities like two-dimensional (2D) strain and 4D echocardiography for early detection of subtle changes in the myocardium.

  Patients and methods Top

Study population

We enrolled an observational case–control study that included 35 patients referred from the Neurology Department, El-Hussein University Hospital, Al-Azhar University with a diagnosis of progressive muscular dystrophy (Duchenne and Becker type) by clinical phenotyping, serum creatinine phosphokinase (CPK) levels, electromyography, genetic testing, and skeletal muscle biopsy in the period from January 2017 to December 2017. Exclusion criteria included muscular dystrophies other than DMD or BMD, presence of LVEF of less than or equal to 50%, chronic illness such as hypertension or diabetes mellitus, renal diseases, pulmonary diseases, congenital, or other preexisting cardiac diseases. All cases were subjected to detailed history taking and thorough clinical examination including anthropometric measures (height, weight) for BMI and body surface area (BSA) calculation, heart rate, blood pressure, and cardiac examination. Twelve-lead surface resting ECG was done for all cases. Five cases were excluded because of severe kyphoscoliosis with poor echogenic window in one of them and the other four of them had an LVEF of less than 50%.

The mean age of patients was 19.73±10.4 years and they were 25 men and five women compared with 30 age-matched and sex-matched healthy individuals as a control group. The patients were divided into group 1 (G1) that included 13 patients with BMD (11 men and two women; mean age, 26.62±12.23 years) and 17 patients with DMD (14 men and three women; mean age, 14.47±3.73 years). Informed oral consent had been obtained from all participants and the study was approved by the ethics committee of Faculty of Medicine for Girls, Al-Azhar University.

Echocardiographic study

2D echocardiography was performed in Cardiology Department, Al-Zahraa University Hospital on all study populations using Vivid E9 (GE Ultrasound, Horten, Norway) ultrasound machine. Cases were examined by a multifrequency (2.5 MHz) matrix probe (M3S). All images were digitally stored for later off-line analysis at Echo PAC.GE Version 201. Comprehensive TTE M-Mode, 2D, Doppler (pulsed and continuous wave), color flow mapping in the standard views (parasternal long axis, parasternal short axis, apical four-, three-, and two-chamber views) from all accessible windows were obtained with ECG physio-signal display and loop recording of two to three cycles. All parameters were taken according to standards of the American Society of Echocardiography to measure LV dimensions and functions [6] including conventional Doppler [mitral valve early diastolic velocity (MV E vel), mitral valve late diastolic velocity (MV A vel), and MV E/A ratio].

Tissue Doppler imaging (TDI) was obtained from apical four-chamber and two-chamber views. For data acquisition, three complete cardiac cycles were collected and stored in a cine loop format. The image sector width was set as narrow as possible to allow a frame rate acquisition of greater than 90 frames/s. Special attention was paid to the color Doppler velocity range setting to avoid any aliasing within the image. The mitral annular systolic velocity (Sa) and mitral annular early diastolic velocity (Ea) by pulsed-wave tissue Doppler was obtained at inferoseptal, lateral, inferior, and anterior annular positions and then average and E/Ea average ratio was calculated.

The LV myocardial performance index (MPI) was measured as an index of LV global function.

The LV longitudinal strain was also assessed using 2D-STE analysis with QRS onset as the reference point, applying a commercially available strain software package to the LV on echo PAC, Version 210. Images were acquired at 70–90 frame/s at end expiration in the apical four-chamber, three-chamber, and two-chamber views. Using the Automated Function Imaging software, a point-and-click approach was utilized to identify three anchor points (two basal and one apical), following which the software tracked the endocardial contour. The LV 2D ST GS% was obtained in all study cases automatically.

Four-dimensional echocardiographic imaging

4D echocardiographic imaging six-beat full-volume 3D data sets (≥30 vol/s) were obtained during breath-holding using Vivid E9 (Vingmed Ultrasound; GE Healthcare) equipped with 4 V transducer. The 12-slice display was used during acquisition to ensure a complete inclusion of the LV in the data set. The 3D data sets were exported to a separate workstation equipped for off-line analysis using the 4DAutoLVQ package (Echo PAC; GE, version 201).

A quad view that displayed the end-diastolic frame was used for manual alignment of the axis and the mitral valve leaflet. Automated border detection and manual correction followed the endocardium throughout the whole cardiac cycle. The 3D data sets were aligned by setting the LV longitudinal axes in the reference end-diastolic frame. On the LV apical long-axis view, the operator sets the landmarks corresponding to the aortic annulus diameter. The software algorithm analyses ultrasound backscatter intensities and adapts a static LV shape model to all the input data, which can be further optimized by the operator. Then, the LV contours are automatically tracked over the entire cardiac cycle using the speckle tracking technology. Optionally, the operator can correct the LV contours identified by the algorithm, if necessary. Next, end-diastolic volume, end-systolic volume, SV, CO, and EF were automatically calculated. Following, LV mass and myocardial strain calculation, the epicardial border was determined for manual adjustment of the region of interest. The values of 3D-derived strain were generated and conferred as strain curves and a color-coded 17-segment bull’s eye plot.

Statistical analysis

Results were analyzed using the SPSS for Windows software (Version 25; IBM SPSS Inc., Armonk, New York, USA). Continuous variables were presented as means and SD while categorical variables were presented as percentages and frequencies. Normality was confirmed then homogeneity by Levene’s test. Univariate analysis for group comparisons were performed using the one-way analysis of variance with Bonferroni post-hoc method, while Kruskal–Wallis test was used between ordinal variables and χ2 for nominal variables. The associations between variables were assessed by Pearson’s r correlation analysis. A P value less than or equal to 0.05 was accepted as statistically significant and P value less than or equal to 0.001 was considered highly significant.

  Results Top

Demographic and clinical characteristics of the studied cases are shown in [Table 1].
Table 1 Baseline demographic and clinical characteristics of the study population

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G2 patients had significantly lower age than G1 patients but no significant difference between groups regarding sex, body weight, systolic blood pressure or diastolic blood pressure.

Patients with DMD were significantly shorter than BMD patients (P<0.001), had lower BSA and BMI (P<0.001 and 0.002, respectively), higher CPK levels (P<0.001) and more positive family history of MD (P<0.001).

Heart rate was significantly higher in G2 compared with G3 (P=0.04).

Twenty-six patients of G2 (52%) and 20 patients of G1 (40%) needed NICU with significant difference between both groups (P=0.03), while none of G3 patients needed it.

Regarding ECG findings, G2 patients had significantly increased amplitude of R wave in V1 and 2 compared with G1 (P<0.001). Eight (47.06%) patients of G2 had Q wave in inferior leads and V5, 6 while none of G1 or 3 had this finding. PR interval was significantly longer in G1 compared with G3 and in G2 compared with G3 (P<0.001).

Six (35.29%) patients of G2 and two (15.39%) patients of G1 had ST-T wave changes with significant difference between both of them (P<0.001) as shown in [Table 2].
Table 2 Twelve-lead surface resting ECG of the studied groups

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Left ventricular study

We found that both interventricular septal thickness in diastole and left ventricular internal dimension in diastole were significantly increased in G1 compared with G2 (P=0.05 and 0.04) while left ventricular internal dimension in systole was significantly more in G1 compared with G3 (P=0.01).

TD-LV MPI was significant in both G1 and G2 compared with G3 (P<0.001).

Nine (52.94%) patients of G2 and three (23.08) patients in G1 had LV systolic dysfunction measured by LV Sa with significant difference between both groups (P<0.001).

Ten (58.82%) patients in G2 and five (38.46%) patients in G1 had LV diastolic dysfunction measured by LV E/Ea with significant difference between both of them and when compared with G3 (P=0.04).

4D-LVEF was significantly lower in G1 and G2 compared with G3 but within normal references (P<0.001).

There was no significant difference between the three groups regarding left ventricular posterior wall thickness in diastole, EF, left ventricle mass index (LVMI), relative wall thickness (RWT), M E velocity, M A velocity, or M E/A as shown in [Table 3].
Table 3 Conventional echocardiographic parameters of left ventricular dimensions and function

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Regarding LV strains (longitudinal, radial, circumferential, or global), we found that LV peak global strain measured by TDI was significantly lower in G1 and G2 compared with G3 (0.002). The only LV strain with significant difference between G1 and G2 was septal strain (P<0.001).

Using 2D-STE, we found that septal strain, lateral strain, anteroseptal, 2D-global longitudinal strain (GLS), and 4D-GLS strains were significantly lower in G1 and G2 compared with G3 (P<0.001, P=0.05, P<0.001, P=0.01, and P<0.001, respectively).

We found that apical, mid, and basal posterior LV strain were significantly lower in G2 compared with G1 (P=0.002, P<0.001 for mid and basal). Also, 2D-GLS was lower in G2 compared with G1 (P≤0.001) as shown in [Table 4] and [Figure 1].
Table 4 Left ventricular longitudinal strain parameters of the studied groups

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Figure 1 Comparison between the three groups regarding apical, mid, basal posterior LV strain, and 2D-GLS. 2D, two-dimensional; GLS, global longitudinal strain; LV, left ventricular.

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Regarding LV radial strain, global radial strain (GRS) was significantly lower in G1 and G2 compared with G3 (P<0.001). The mid and basal septal strain and basal posterior strain were significantly lower in G2 compared with G1 (P<0.001 for all).

Global circumferential strain (GCS) was significantly lower in G1 and G2 compared with G3 (P<0.001) while the mid and basal posterior strains were significantly lower in G2 compared with G1 (P<0.001) as shown in [Figure 2]a and b.
Figure 2 Comparison between the studied groups regarding a GRS, mid, and basal posterior strain. GRS, global radial strain.

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We found positive correlation between serum CPK levels and TD-LV MPI while negative correlation between CPK levels and GRS and GCS as shown in [Table 5].
Table 5 Correlation between creatinine phosphokinase and different echocardiographic parameters of left ventricular assessment

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We found also a positive correlation between the amplitude of R wave in leads V1 and V2 in ECG and LVMI and RWT while negative correlation between R and longitudinal mid-posterior LV strain, longitudinal basal posterior strain, and GCS as shown in [Table 6].
Table 6 Correlation between R wave in ECG and different echocardiographic parameters of left ventricular assessment

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We plotted the receiver-operating characteristic curve to define the cutoff value of serum CPK level that can predict LV affection in patients with progressive muscular dystrophies (BMD and DMD). We found that the value was 144.5 mg with area under the curve=0.768, 92% sensitivity, and 63% specificity (P=0.003) ([Figure 3]).
Figure 3 ROC curve representing serum level CPK that can predict LV dysfunction in BMD and DMD. BMD, Becker’s muscular dystrophy; CPK, creatinine phosphokinase; DMD, Duchenne muscular dystrophy; LV, left ventricular; ROC, receiver-operating characteristic.

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  Discussion Top

The muscular dystrophies are a heterogeneous group of conditions with variable distribution and prognosis. Cardiac complications are common and may significantly alter both quality and quantity of life [7].

DMD is the most common inherited lethal childhood muscle disorder, affecting one in 5000 live newborn men. It is an X-linked recessive disease caused by alterations of the DMD gene that results in deficiency of the dystrophin protein which links the actin cytoskeleton to the basal lamina via the dystrophin–glycoprotein complex and is essential for normal muscle function [8].

BMD prevalence is about one-third that of DMD affecting one in 18 450 male live births and caused by reduced levels or abnormal variants of dystrophin, rather than the absent levels seen in DMD and again is transmitted in an X-linked recessive pattern [9].

The same pathophysiology occurring in skeletal muscles also affect the cardiac muscle; however, the sedentary life of those patients may place minimal stress on the heart thus making CM asymptomatic [8].

DMD patients had a lower age compared with BMD which is as expected because the life expectancy in DMD is between 15 and 25 years while patients with BMD may be asymptomatic till the age of 30 or 40 years [10].

Both DMD and BMD are X-linked diseases that affect usually men but rarely affect women and women may be carriers [11]. Women in our study were five from which one of them had DMD and the other four were carriers.

Our study showed that patients with DMD had smaller BSA and BMI and higher heart rate compared with both BMD and controls. That was explained by Romfh and McNally [5], in their review as they mentioned that those patients had loss of weight, nausea, palpitation, and sleep disturbances.

Higher CPK levels in DMD represent the more aggressive nature of the disease.

We found that 47.08% of DMD patients had Q waves in inferior leads, LI, aVL, V5, V6 in the surface ECG with taller R wave in V1 and V2 compared with BMD that was nearly concordant to Thrush et al. [12], who studied 115 boys with DMD and demonstrated that ECG changes occurred in about half of the patients.

Perlof [13] reported that postmortem studies revealed selective scarring at the posterobasal region of the heart owing to the loss of posteriorly directed forces and creating electrically silent regions and tall precordial R waves.

We reported that TD-LV MPI was higher in both DMD and BMD patients in concordance to the study by Shabanian et al. [14], who found the same results in their research concluding that MPI might be helpful for early detection of silent cardiac affection in DMD patients when other conventional echocardiographic parameters are within the normal limits.

We demonstrated that LV E/Em was higher in both G1 and G2 compared with controls which is reported in the Markham et al. [15] review as echocardiographic evidence of diastolic dysfunction precedes the development of dilated cardiomyopathy and applies to other dystrophinopathies such as BMD and female carriers.

Strain imaging is another echocardiographic modality that can detect early LV involvement despite normal LVEF.

We found that septal, lateral, and global LV strain measured by TDI were lower in patients than control.

With the more recent 2D-STE we can detect not only GLS affection, but also segmental, circumferential, and radial strain affection.

We found that GLS, GRS, and GCS were affected in our patients compared with control. In addition, segmental analysis revealed that the most affected wall in the LV of DMD was mid and basal posterior segments even compared with BMD. Septal and lateral walls were affected in both types of muscular dystrophies.

Mori et al. [16] reported that strain imaging of DMD patients is characterized by a decreased peak systolic strain of the posterior wall despite normal standard echocardiographic findings and explained this finding by the fact that myocardial fibrosis is initially localized to the posterobasal part of the LV free wall, followed by the development of interventricular septum and right ventricular fibrosis.

We found that 4D-LVEF and 4D-LV-GLS were lower in patients compared with control. However, 4D-LVEF values were within normal references that did not add much data to 2D-TTE but 4DE may have a role in the future.

Differences in segmental strain were found to be predictive of outcome, thereby identifying a patient’s risk for early progression of myocardial dysfunction and death. Thus, in younger patients with normal systolic function as detected by echocardiography, it may be important to pair echocardiographic evaluations with additional forms of imaging.

Women in our study were five (83.33%) diagnosed as carriers, three (60%) of them showed ECG and echocardiographic evidences of LV diastolic and systolic dysfunction which is nearly concordant with the study by Song et al. [17], who reported 55% cardiac involvement in female carriers.We reported a positive correlation between CPK as an indicator of muscle destruction and global LV function measured by MPI while negative correlation with GRS and GCS in concordance with the study by Posner et al. [18], who concluded a possible association between skeletal and cardiac muscle function and suggests that researchers should carefully monitor cardiac function, even when the primary outcome measures are not cardiac in nature.

Also, we found a positive correlation between the amplitude of R wave in V1, V2 in surface ECG with LVMI and RWT while negative correlation with GCS, longitudinal MPS and BPS that may point to the importance of ECG in early detection of cardiac changes.

Thrush et al. [12] studied the correlation between precordial R wave and LV dimensions and EF in DMD and found no relation in agreement with our study. However, they did not study strain or LVMI so further studies are needed to confirm this relation.

When we plotted receiver-operating characteristic curve to determine the level of CPK that can predict LV dysfunction, we found that a CPK level of 144.5 has P value=0.003 with 92% sensitivity and 63% specificity reflecting that the continuous and more the destruction of skeletal muscle, the more the cardiac muscle affection.

Limitations and strengths

We did not study the outer versus inner layers of myocardium and we did not involve cardiac MRI in the study as the gold standard imaging modality for tissue characterization, scar and fibrosis detection and volume assumption.

  Conclusion Top

We concluded that recent echocardiographic modalities as 2D-STE can detect early and subtle cardiac involvement in patients with muscular dystrophies as DMD and BMD for early treatment and prevention of cardiac complications.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Silvestri NJ, Ismail H, Zimetbaum P, Raynor EM. Cardiac involvement in the muscular dystrophies. Muscle Nerve 2018; 57:707–715.  Back to cited text no. 1
Romitti PA, Zhu Y, Puzhankara S, James KA, Nabukera SK, Zamba GKD et al. Prevalence of Duchenne and Becker Muscular dystrophies in the United States. Pediatrics 2015; 135:512–521.  Back to cited text no. 2
Yilmaz A, Gdynia HJ, Baccouche H, Mahrholdt H, Meinhardt G, Basso C et al. Cardiac involvement in patients with Becker muscular dystrophy: New diagnostic and pathophysiological insights by a CMR approach. J Cardiovasc Magn Reson 2008; 10:1–12.  Back to cited text no. 3
Soslow JH, Xu M, Slaughter JC, Stanley M, Crum K, Markham LW et al. Evaluation of echocardiographic measures of left ventricular function in patients with duchenne muscular dystrophy: assessment of reproducibility and comparison to cardiac magnetic resonance imaging. J Am Soc Echocardiogr 2016; 29:983–991.  Back to cited text no. 4
Romfh A, McNally EM. Cardiac assessment in duchenne and becker muscular dystrophies. Curr Heart Fail Rep 2010; 7:212–218.  Back to cited text no. 5
Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al. Recommendations for cardiac chamber quantification by echocardiography in adults: An update from the American society of echocardiography and the European association of cardiovascular imaging. Eur Heart J Cardiovasc Imaging 2015; 16:233–271.  Back to cited text no. 6
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Thrush PT, Edward N, Flanigan KM, Mendell JR, Allen HD. Precordial R wave height does not correlate with echocardiographic findings in boys with duchenne muscular dystrophy. Congenit Heart Dis 2013; 8:561–567.  Back to cited text no. 8
Bushby KMD, Thambyayah M, Gardner-Medwin D. Prevalence and incidence of Becker muscular dystrophy. Lancet 1991; 337:1022–1024.  Back to cited text no. 9
Mathieu J, Allard P, Potvin L, Prévost C, Bégin P. A 10-year study of mortality in a cohort of patients with myotonic dystrophy. Neurology 1999; 52:1658–1662.  Back to cited text no. 10
Ishizaki M, Kobayashi M, Adachi K, Matsumura T, Kimura E. Female dystrophinopathy: review of current literature. Neuromuscul Disord 2018; 28:572–581.  Back to cited text no. 11
Thrush PT, Allen HD, Viollet L, Mendell JR. Re-examination of the electrocardiogram in boys with duchenne muscular dystrophy and correlation with its dilated cardiomyopathy. Am J Cardiol 2009; 103:262–265.  Back to cited text no. 12
Perloff JK. Cardiac rhythm and conduction in Duchenne’ s muscular dystrophy. J Am Coll Cardiol 1984; 3:1263–1268.  Back to cited text no. 13
Shabanian R, Aboozari M, Kiani A, Seifirad S, Zamani G, Nahalimoghaddam A et al. Myocardial performance index and atrial ejection force in patients with Duchenne’s muscular dystrophy. Echocardiography 2011; 28:1088–1094.  Back to cited text no. 14
Markham LW, Michelfelder EC, Border WL, Khoury PR, Spicer RL, Wong BL et al. Abnormalities of diastolic function precede dilated cardiomyopathy associated with duchenne muscular dystrophy. J Am Soc Echocardiogr 2006; 19:865–871.  Back to cited text no. 15
Mori K, Hayabuchi Y, Inoue M, Suzuki M, Sakata M, Nakagawa R et al. Myocardial strain imaging for early detection of cardiac involvement in patients with Duchenne’s progressive muscular dystrophy. Echocardiography 2007; 24:598–608.  Back to cited text no. 16
Song T, Lee K, Kang S, Cho H, Choi Y. Three cases of manifesting female carriers in patients with duchenne muscular dystrophy. Yonsei Med J 2019; 52:192–195.  Back to cited text no. 17
Posner AD, Soslow JH, Burnette WB, Bian A, Shintani A, Sawyer DB et al. The Correlation of skeletal and cardiac muscle dysfunction in Duchenne muscular dystrophy. J Neuromuscul Dis 2016; 3:91–99.  Back to cited text no. 18


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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