Myocardial Strain Assessment for Early Duchenne Muscular Dystrophy Diagnosis in Pediatric Patients Using Cardiac MRI

Abstract

Assessing myocardial strain remains challenging, particularly in the pediatric population, due to the smaller heart sizes, higher heart rates, and variability in strain parameters compared to adult populations. This study aimed to investigate the utility of myocardial strain measurements using cardiac magnetic resonance-feature tracking (CMR-FT) for early diagnosis of Duchenne muscular dystrophy (DMD) in pediatric patients. Twenty-eight DMD patients and 20 healthy controls were involved in this study. Global circumferential, longitudinal, and radial strain (GCS, GLS, and GRS) were measured for the left ventricle (LV) using CMR-FT. Segmental strain values only of the inferolateral and anterolateral LV segments in DMD patients without late gadolinium enhancement (LGE) and DMD patients with LGE were compared to the healthy controls. Strain measurements using CMR-FT in DMD patients were considerably lower than those of healthy controls, with all p-values lower than 0.001. DMD patients without LGE showed decreased inferolateral and anterolateral segmental values only relative to healthy controls. The same behavior was maintained for the LV geometry. Multivariable linear regression demonstrated that the end-systole (ES) wall thicknesses and thickening were associated with decreased GCS and GLS. CMR-FT is crucial in detecting cardiac abnormalities in patients with DMD. It represents an innovative imaging biomarker that can detect initial myocardial alterations in DMD cardiomyopathy without relying on gadolinium.

1. Introduction

Myocardial strain represents a critical parameter for quantifying myocardial deformation throughout the cardiac cycle [1]. It provides detailed insights into the heart’s mechanical function, particularly that of the myocardium, which is the heart’s muscular tissue. The three primary strain categories are circumferential, radial, and longitudinal, which can be measured to reflect different aspects of cardiac function impairment [2]. Circumferential strain assesses deformation around the heart’s circumference, radial strain evaluates myocardial thickening, and longitudinal strain examines changes along the length of the heart. Each component offers unique insights into myocardial performance and potential dysfunction [3,4]. Strain measurements have demonstrated the ability to detect overall and localized myocardial dysfunction, distinguish between various types of cardiac diseases, and serve as an earlier indicator of myocardial disease compared to ejection fraction (EF) [5].

Various imaging techniques have been developed to evaluate myocardial strain and further refine the assessment of ventricular function, considering the intricate architecture of the heart [6,7]. Among these imaging techniques, transthoracic echocardiography (TTE) is the principal imaging modality for assessing myocardial strain primarily because of its widespread availability, ease of use, and non-invasive nature [8]. Advanced imaging techniques such as speckle tracking echocardiography (STE) and three-dimensional echocardiography offer detailed and accurate assessments of myocardial strain, providing valuable insights into myocardial function [9]. However, these modalities have limitations that can affect their application in clinical settings. These include the angle dependency of tissue Doppler ultrasound, the limitations of the acoustic window, and the precision and reproducibility of echocardiographic measurements, including strain imaging, which can vary significantly based on the operator’s experience and skill [1].

Cardiac magnetic resonance (CMR) imaging is often regarded as the primary method for analyzing myocardial strain due to its superior image quality, high spatial resolution, and comprehensive assessment capabilities [10,11,12]. Cardiac magnetic resonance-feature tracking (CMR-FT) is an emerging technique that uses cine images acquired during routine CMR imaging. This technique involves following the actual boundary of the myocardium over time, enabling assessment of myocardial strain and motion without using contrast agents. Moreover, CMR-FT offers a non-contrast alternative to imaging techniques such as STE. For this reason, myocardial strain measurement is widely used in medical imaging diagnostics. It provides advantages over STE in terms of superior image quality. CMR-FT reports significantly fewer non-analyzable segments and larger fields of view compared to STE. This is particularly beneficial in patients with suboptimal echocardiogram image quality due to ultrasound dropouts, reverberations, or poor imaging windows [13,14]. In the literature, several studies have explored the use of strain analysis in CMR image analysis [15,16,17,18]. These studies primarily focus on myocardial strain in healthy and pathological adults, providing valuable insights into various cardiovascular conditions and the effectiveness of different treatments. However, the research on myocardial strain in pediatric populations is still limited. The unique physiological and developmental characteristics of children’s hearts require specialized approaches and normative data for accurate assessment. Expanding studies to include pediatric populations is crucial for improving the diagnosis and treatment of congenital heart diseases and other pediatric cardiac conditions. Thus, some studies were dedicated to improving the importance of strain analysis in the pediatric population focused on the early diagnosis of Duchenne muscular dystrophy (DMD) cardiomyopathy [19,20,21,22,23,24].

Table 1. An overview of state-of-art research works.

Study	Number of Subjects (n)	Modality	Technique	Strain Measurements
Hor et al. (2009) [19]	70 DMD/16 controls	MRI	HARmonic Phase	${\epsilon }_{cc}$
Taqatqa et al. (2016) [20]	19 DMD/16 controls	Echocardiography	STE	GCS/GLS
Siegel et al. (2017) [21]	24 DMD/8 controls	MRI/Echocardiography	FT/STE	GCS
Oreto et al. (2020) [22]	32 DMD/24 controls	Echocardiography	STE	GCS/CLS
Panovsky et al. (2021) [23]	51 DMD/18 controls	MRI/Echocardiography	FT/MAPSE	GCS/GLS/GRS
Prakash et al. (2022) [24]	38 DMD	MRI/Echocardiography	TTE/STE/TDI	GS
Our study (2024)	28 DMD/20 controls	MRI	FT	GCS/GLS/GRS

ε_cc: Circumferential strain, DMD: Duchenne muscular dystrophy, MRI: magnetic resonance imaging, STE: speckle tracking echocardiography, GCS: global circumferential strain, GLS: global longitudinal strain. FT: feature tracking, MAPSE: mitral annular plane systolic excursion, GRS: global radial strain, TTE: transthoracic echocardiography, TDI: tissue Doppler imaging.

presents an overview of various authors’ research over different periods. Each study included a distinct number of participants (n) and used different techniques to measure strain with different modalities providing detailed measurements. DMD is a rare and severe genetic disorder marked by muscle degeneration and weakness, impacting both skeletal and cardiac muscles [25]. It is caused by a mutation in the gene encoding the dystrophin protein, and it stands as the most prevalent and severe form of muscular dystrophy, impacting 1 (one) in every 5000 male births globally [26].

The early detection of cardiac complications in DMD remains a significant challenge [27]. For example, Hor et al. [19] hypothesized that the global circumferential strain (GCS) of the left ventricle (LV) would decrease in DMD before the onset of clinical symptoms. They evaluated CMR imaging in a cohort comprising 17 DMD patients and 16 healthy controls. They analyzed the tagged images with the HARmonic Phase technique for the myocardial strain measurements. Additionally, the research work of Taqatqa et al. [20] investigated the role of STE in detecting the earliest signs of impaired cardiac function in DMD patients. For instance, Siegel et al. [21] conducted a study using CMR-FT and STE techniques in DMD patients and aged-matched controls to measure the strain. In 2020, the research of Oreto et al. [22] examined echocardiographic and clinical data. The researchers demonstrated that the global longitudinal strain (GLS) was noticeably impaired in apical segments and the posterolateral wall, while there was a notable decrease in the GCS observed specifically in the anteroseptal, anterior, and anterolateral segments in older patients. Then, Panovsky et al. [23] conducted a study employing CMR strain analysis and mitral annular plane systolic excursion (MAPSE) to detect the earliest LV dysfunction in DMD patients. This study evaluated three categories of patients: the first category included patients with gadolinium enhancement (LGE) and left ventricle ejection fraction (LVEF) < 50%, the second category was patients with LGE and LVEF ≥ 50%, and the last category patients without LGE and LVEF ≥ 50%. The first and second categories had significantly lower GCS, GLS, global radial strain (GRS) values, and MAPSE than controls. This research has highlighted significant advances, proving that MAPSE and FT measurements allow precise evaluation of early cardiac impairment in DMD patients. A recent study by Prakash et al. [24] compared CMR imaging with transthoracic echocardiography (TTE), incorporating tissue Doppler imaging (TDI) and speckle tracking echocardiography for the early diagnosis of cardiomyopathy in DMD patients. These studies [19,20,21,22,23,24] have shown that the CMR imaging technique provides significant results for DMD diagnosis compared with the STE technique. Nevertheless, these results can still be improved, as research on myocardial strain in pediatric populations remains limited.

Hence, this research work aimed to expand the use of CMR-FT to evaluate global circumferential, longitudinal, and radial strain of the LV, as well as segmental strain at two specific levels, anterolateral and inferolateral, in DMD patients, and to compare these measurements with those of age-matched healthy controls. The main contributions of the current research are the following.

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A dataset was collected for this study that comprised data of 28 DMD patients and 20 healthy controls.

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Exploration of the utility of myocardial strain measurements: This study is among the first to explore the utility of cardiac magnetic resonance-feature tracking (CMR-FT) for early diagnosis of Duchenne muscular dystrophy (DMD) in pediatric patients, a population where early detection is crucial for timely intervention.

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Our research highlights the use of CMR-FT in detecting myocardial strain abnormalities in DMD patients without relying on late gadolinium enhancement (LGE).

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Investigation of the association of LV geometry with strain parameters.

2. Materials and Methods

2.1. Study Population

Twenty-eight patients diagnosed with DMD in the Pediatric Neurology department of the National Institute Mongi Ben Hmida of Neurology, in Tunisia, and twenty aged-gender-matched healthy subjects were qualified in this cross-sectional study. All patients underwent CMR imaging between January and September 2024 at the Principal Military Hospital of Instruction of Tunis (PMHT) in Tunisia. Patients with clinical symptoms of cardiovascular disease, coexisting conditions such as autism syndrome, hyperactivity, claustrophobia to MRI, and diagnosed with muscular dystrophy disease other than DMD were excluded. The study was approved by the Ethical Committee of PMHT, and permission consent was signed by all patients’ parents before the CMR imaging.

2.2. MRI Acquisition and Data Analysis

A 1.5 Tesla MR system (SIGNA Artist, GE Healthcare) was used to acquire all CMR images. The routine measurement was carried out using a standard balanced steady state-free precession (SSFP) cine image technique with a retrospective electrocardiogram (ECG) gating and the calculation of cardiac output using a segmented free-breathing fast imaging employing steady-state acquisition (FIESTA) sequence. Free-breathing sequences were used instead of breath-holding sequences wherever possible due to the difficulty of breath-holding for children, especially those with DMD [28]. The parameters of the scan were as follows: repetition time (TR)/echo time (TE) = 4.1 ms/1 ms, flip angle = 50°, slice thickness = 8 mm, matrix = 192 × 160 pixels, and field of view (FOV) = 270 × 100 mm². Late gadolinium enhancement (LGE) sequences were realized 10 min after gadolinium injection using two LGE sequences to maximize the detection of myocardial fibrosis. Single-shot myocardial delayed enhancement (SS-MDE) sequence in short-axis view and free-breathing phase-sensitive inversion-recovery (PSIR) views were used (Figure 1). For the SS-MDE sequence, the used parameters were TR/TE = 3.8 ms/1 ms, flip angle = 40°, slice thickness = 8 mm; matrix = 160 × 128 pixels and field of view 280 × 100 mm²; for the PSIR sequence, TR/TE = 3.9 ms/1 ms, flip angle = 45°, slice thickness = 8 mm, matrix = 160 × 128 pixels, and field of view 280 × 100 mm².

The images underwent analysis utilizing Circle Cardiovascular Imaging (CVI42) software (Calgary, Alberta, Canada). The structure and function of both the left and right ventricles were measured on short-axis cine images. Endocardial and epicardial contours were applied during the end-systole (ES) and end-diastole (ED) phases. Manual verification and correction of phases and contours were then performed. Papillary muscles were not considered in the assessment of ventricular volume. The following cardiac measurements were obtained: LV volumes and ejection fraction.

CMR-FT measurements were performed in the post-processing phase after the specified study was finished using CVI42. Thus, using cine images and endocardium and epicardium contours were identified along the cardiac cycle for short- and long-axis slices (Figure 1). The basal level was obtained by slicing the heart horizontally near its base, including the ventricles’ upper sections. The mid-ventricular level was taken at a specific cross-section of the heart, usually around the papillary muscles. The apical level was taken at the apex, the lower tip of the heart. The GCS and GRS were analyzed in short-axis slices (basal, mid-ventricular, and apical), and the GLS was assessed in long-axis slices (2-chamber, 3-chamber, 4-chamber).

2.3. Statistical Analysis

The demographic data, CMR characteristics, and strain measurements were analyzed and compared between DMD patients and healthy controls using Student’s t-test. The numerical and percentage equations were used for categorical variables, while continuous variables were represented as mean ± standard deviation.

Statistical significance was defined as a p-value <0.05. The diagnostic performance of these parameters was subsequently evaluated using probability statistics, receiver operating characteristic (ROC), and areas under the curve (AUC) analysis. For the GCS, GRS, and GLS, 95% confidence intervals (CIs) were determined. All analyses were performed using the statistical software IBM^® SPSS ^® (version 23.0, IBM SPSS Inc., Chicago, IL, USA).

3. Results

3.1. Subject Characteristics

Forty-eight subjects, 28 DMD patients and 20 healthy controls, were included in this study. The studied subjects’ demographic data are presented in Table 2. The average age of the healthy controls was 11.85 ± 2.81 (IQR 6–15) years. For the DMD patients, the mean age was 10.56 ± 2.60 (IQR 5–16) years. Weight, height, and body surface area (BSA) were significantly lower for DMD patients (all p ≤ 0.001). The DMD patients had lower weight (33.89 ± 10.97 kg vs. 46.27 ± 12.93 kg), height (132 ± 10.68 cm vs. 147.75 ± 16.96 cm), and body surface area (1.12 ± 0.32 m² vs. 1.42 ± 0.28 m²) than healthy controls.

3.2. CMR Characteristics

3.2.1. Functional and Geometry

All volumes were indexed to body surface area (BSA) using the Boyd equation. The measured CMR parameters are presented in Table 2. In general, no significant variation was observed in left ventricle end-systole volume (LVESV), left ventricle end-diastole volume (LVEDV), left ventricle stroke volume (LVSV), and myocardial mass between the DMD patients and controls (all p-value > 0.05). However, there were significant differences in left and right ventricular EF parameters, with notably lower values in the DMD patients than in healthy controls. The mean of LVEF for the healthy controls was 61.60 ± 40.60 (IQR 53–72) %. For the DMD patients, the mean of LVEF was 56.14 ± 3.51 (IQR 50–65) %, (p-value <0.05). A value of 38% of all DMD patients showed a lower LVEF (<55%). Based on the dataset studied, ED wall thickness, ES wall thickness, and ED wall thickening from the basal to the apical level of the LV were calculated for the healthy controls and DMD patients. The mean ED wall thickness was 8.81 ± 1.76 mm in the healthy controls and 6.72 ± 2.71 mm in the DMD patients. The ES wall thickness was 8.89 ± 2.52 mm in the healthy controls and 7.38 ± 2.75 mm in the DMD patients. The average value of wall thickening was 72.83 ± 7.47% in the healthy controls and 55.85 ± 8.98% in the DMD patients.

Table 2. Subjects’ demographic, clinical, and CMR characteristics.

Variable	DMD (n = 28)	Controls (n = 20)	p-Value
Subject characteristics
Age (year)	10.56 ± 1.79	11.30 ± 2.71	0.057
Weight (kg)	31.36 ± 6.45	42.85 ± 12.73	0.001
Height (cm)	133.29 ± 10.56	148.45 ± 14.74	<0.001
BSA (m2)	1.06 ± 0.15	1.34 ± 0.25	<0.001
CMR characteristics of LV Functional
LVEDV/BSA (mL/m2)	73.07 ± 10.74	80.09 ± 6.80	0.887
LVESV/BSA (mL/m2)	33.07 ± 5.58	30.87 ± 4.69	0.150
SV/BSA (mL/m2)	41.96 ± 7.65	48.48 ± 7.06	0.005
Myocardial mass/BSA (g/m2)	40.54 ± 4.80	40.20 ± 5.25	0.820
LVEF (%)	56.14 ± 3.51	61.60 ± 4.66	0.003
Geometry
ED wall thickness (mm)	6.72 ± 2.71	8. 18 ± 1.76	<0.001
ES wall thickness (mm)	7.38 ± 2.75	8.89 ± 2.52	<0.001
Wall thickening (%)	55.85 ± 8.98	72.83 ± 7.45	<0.001

BSA: body surface area; LVESV: left ventricle end-systole volume; LVEDV: left ventricle end-diastole volume; SV: stroke volume; ED: end diastole; ES: end-systole; LVEF: left ventricle ejection fraction; data are presented as means ± SD (significant p-values are indicated in bold).

Table 2. Subjects’ demographic, clinical, and CMR characteristics.

Variable	DMD (n = 28)	Controls (n = 20)	p-Value
Subject characteristics
Age (year)	10.56 ± 1.79	11.30 ± 2.71	0.057
Weight (kg)	31.36 ± 6.45	42.85 ± 12.73	0.001
Height (cm)	133.29 ± 10.56	148.45 ± 14.74	<0.001
BSA (m2)	1.06 ± 0.15	1.34 ± 0.25	<0.001
CMR characteristics of LV Functional
LVEDV/BSA (mL/m2)	73.07 ± 10.74	80.09 ± 6.80	0.887
LVESV/BSA (mL/m2)	33.07 ± 5.58	30.87 ± 4.69	0.150
SV/BSA (mL/m2)	41.96 ± 7.65	48.48 ± 7.06	0.005
Myocardial mass/BSA (g/m2)	40.54 ± 4.80	40.20 ± 5.25	0.820
LVEF (%)	56.14 ± 3.51	61.60 ± 4.66	0.003
Geometry
ED wall thickness (mm)	6.72 ± 2.71	8. 18 ± 1.76	<0.001
ES wall thickness (mm)	7.38 ± 2.75	8.89 ± 2.52	<0.001
Wall thickening (%)	55.85 ± 8.98	72.83 ± 7.45	<0.001

BSA: body surface area; LVESV: left ventricle end-systole volume; LVEDV: left ventricle end-diastole volume; SV: stroke volume; ED: end diastole; ES: end-systole; LVEF: left ventricle ejection fraction; data are presented as means ± SD (significant p-values are indicated in bold).

3.2.2. Strain Measurements

An example of strain measurements using the CMR-FT technique of a DMD patient is illustrated in Figure 2. As

Table 3. Left ventricular myocardial strain parameters of subjects.

Variable	DMD (n = 28)	Controls (n = 20)	p-Value
GCS (%)	−16.12 ± 3.55	−19.34 ± 4.48	<0.001
GLS (%)	−13.79 ± 5.28	−17.13 ± 5.94	<0.001
GRS (%)	27.49 ± 2.44	31.69 ± 2.53	<0.001

(Significant p-values are indicated in bold).

indicates, the CMR-FT strain measurements were considerably lower than those of the healthy controls. All p-values were lower than 0.001. The average GCS found was −16.12 ± 3.55%, IQR [−19.40, −13.00] % vs. −19.34 ± 4.48%, IQR [−21.70, −16.40] %. The GLS was reduced in the DMD patients in comparison to the healthy controls: (−13.79 ± 5.28%, IQR [−16.90, −11.40] % vs. –17.13 ± 5.94%, IQR [−18.40, −12.50] %). The same behavior was maintained for the GRS of the DMD patients: 27.49 ± 2.44%, IQR [23.20, 35.90] % and for the healthy controls: 31.69 ± 2.53%, IQR [25.90, 35.00] %. ROC curve analysis was applied to evaluate the capability of global strain measurements to differentiate the DMD patients from the healthy controls (Figure 3 and

Table 4. ROC analysis results.

Variable	AUC (95% CI)	p-Value	Sensitivity (%)	Specificity (%)
GCS (%)	0.93	0.003	86	90
GLS (%)	0.98	0.001	96	95
GRS (%)	0.94	0.046	90	93

). The GCS, GLS, and GRS performed well, providing areas under the curve (AUC) values of 0.93, 0.98, and 0.94, respectively. The values of p-value, sensitivity, and specificity of the different global strain measurements are presented in Table 4. Among these parameters, the GCS exhibited the highest sensitivity (86%), with a specificity of 90%, while the GLS demonstrated the highest specificity (96%), with a sensitivity of 95%. Moreover, the GRS showed specificity and sensitivity levels surpassing 90%. The AUC for the GLS was the greatest (0.98, p-value = 0.001), despite the GLS to GRS on the long axis (LAX) exhibiting a gradual increase in the AUC.

3.3. Correlation Between Myocardial Strain and LGE Assessment

The LGE was positive in 16 DMD patients, defining LGE+ group. Meanwhile, 12 DMD patients presented no evidence of LGE defining the LGE− group. Comparisons of strain measurements within the anterolateral and inferolateral segments of the LV among the LGE+ and LGE− groups were conducted relative to the healthy controls (

Table 5. Segmental strain comparison between the healthy controls and DMD patients with and without LGE.

Segment	Controls (n = 20)	LGE− (n = 12)	LGE+ (n = 16)	p-Value
Circumferential strain (%)
Anterolateral	−20.23 ± 1.85	−15.32 ± 1.32	−13.80 ± 1.78	0.033
Inferolateral	−20.78 ± 1.70	−14.05 ±1.79	−13.49 ± 1.65	0.042
Longitudinal strain (%)
Anterolateral	−18.58 ± 2.79	−14.86 ± 1.41	−12.89 ± 1.85	0.046
Inferolateral	−16.94 ± 2.37	−13.93 ± 1.80	−13.42 ± 1.62	0.040
Radial strain (%)
Anterolateral	29.72 ± 2.58	26.18 ± 2.45	24.32 ± 1.55	0.043
Inferolateral	28.10 ± 3.53	24.89 ± 1.93	23.74 ± 2.21	0.030

). Additionally, a box plot was generated to illustrate the difference in global strain between the healthy controls and the LGE+ and LGE− groups (Figure 4). A significant difference was found between the healthy controls and the LGE− group in the anterolateral circumferential strain (p-value = 0.033) and the inferolateral circumferential strain (p-value = 0.042) values. Findings were similar regarding the longitudinal and radial strain in anterolateral and inferolateral segments (all p-values < 0.05). CMR-FT analysis of the inferolateral and anterolateral segments identified notable disparities between the healthy controls and those without LGE. Based on the results, the inferolateral and anterolateral segments were the most affected segments. Figure 5 shows a bull’s-eye diagram illustrating the distribution of strain across 16 segments of the LV. In this diagram, myocardial segments in DMD patients are indicated in red, while those in healthy controls are in blue.

3.4. Correlation Between Global Strain Parameters and LV Geometry

The correlation between the myocardial global strain and the LV geometry values is indicated in

Table 6. Results of the multivariable linear regression of the myocardial global strain.

Variable	GCS (%)		GLS (%)		GRS (%)
	β	p-Value	β	p-Value	β	p-Value
ES wall thickness (mm)	−0.26	0.002	−0.09	0.003	0.06	0.82
ED wall thickness (mm)	0.20	0.319	−0.06	0.730	0.03	0.92
Wall thickening (%)	−0.30	0.010	−0.29	0.040	0.08	0.78

β: standardized coefficients (beta). Significant p-values are indicated in bold.

. A multivariable linear regression demonstrated that ES wall thickness and wall thickening (%) were associated with decreased GCS and GLS (β = −0.26 and −0.30, p-value < 0.05) but were not significantly associated with GRS p > 0.05. There was no significant correlation between ED wall thickness and the GCS, GLS, or GRS (all p-values > 0.05).

4. Discussion

This study evaluated left ventricular strain measurements using the CMR-FT technique to describe the utility of myocardium strain assessment for early diagnosis in pediatric patients, especially to detect subclinical cardiac abnormalities in DMD patients without cardiac symptoms. The method used the automatic segment LV contours at both the end-systole and end-diastole phases using the CVI42 software. Then, the CMR-FT technique was used to analyze the GCS, GRS, and GLS, since this technique can provide comprehensive insights into the myocardial function and mechanical deformation of the heart in different phases of the cardiac cycle. The LV volumes and EF were measured using endocardium and epicardium contours during the ED and ES phases without including papillary muscles. A comparative analysis was carried out with existing studies to assess the performance and demonstrate the clinical contribution of the proposed work.

The average age of the healthy controls was 11.30 ± 2.72 years. The cardiac functions and volumes indexed to BSA were normal. The average age of the DMD population was 10.56 ± 1.79 years. The DMD patients had normal cardiac chamber volumes. At the same time, the mean LVEF of the DMD boys was at the lower standard limit: 56.14 ± 3.51%. All DMD patients had statistically significantly lower weight, height, and body surface area than the healthy controls. Various studies showed the same finding [19,20,21,22,23,24]. This is explained by a reduced growth velocity in DMD boys [19]. The current study has revealed that DMD patients exhibit decreased GCS, GLS, and GRS compared to healthy controls. For example, Siegel et al. [21] revealed that DMD cardiomyopathy is associated with a notable decline in the GCS. The mean GCS assessed via CMR-FT was considerably lower in the DMD patients than in the controls: −18.8 ± 6.1% vs. −25.5 ± 3.2%; p-value < 0.05, with notable variations observed at anterolateral, inferolateral, as well as inferior segments. A related study has highlighted the myocardial strain as an important marker of myocardial dysfunction in individuals with DMD using CMR-FT [23]. In comparison, the current study achieved for the DMD patients a GCS of −16.71 ± 4.18% vs. −16.12 ± 3.55%, GLS: − 14.9 ± 41.91% vs. −13.79 ± 5.28% and GRS: 38.3 ± 9.80% vs. 27.24 ± 2.44. Another research study by Siddiqui et al. [25] performed a study using CMR in 30 DMD-associated cardiomyopathy and 30 age-matched DMD patients without associated cardiomyopathy patients. They proved that before DMD-associated cardiomyopathy onset, GRS and GCS were significantly lower in DMD-associated cardiomyopathy compared with DMD without associated cardiomyopathy (25.1 ± 6.0 vs. 29.0 ± 6.3, p = 0.011; −15.4% ± 2.4 vs. −17.3% ± 2.6, p = 0.003). The study suggest that cardiac MRI strain analysis is a valuable tool for predicting the onset of DMD-associated cardiomyopathy. Additionally, a study on DMD patients compared CMR imaging with TTE, including TDI and STE, for diagnosing cardiomyopathy in boys with DMD at an early ambulatory stage [24]. The results demonstrated that the DMD patients exhibited noticeably lower GCS and GLS than the controls: GCS: −14.7 ± 4.7% vs. −23.1 ± 2.9%, GLS: −13.6 ± 5% vs. −18.8 ± 3%, respectively (all p-values < 0.001). Eighteen (56%) DMD patients presented LGE, while fourteen (44%) DMD patients presented no evidence of LGE and the DMD LGE− group showed decreased segmental values only in inferolateral and anterolateral segments compared to the healthy controls. A recent research study by Earl et al. [26] employed a novel 4D CMR regional strain analysis to assess 40 pediatric Duchenne patients across three consecutive annual visits. The results revealed that peak systolic strain served as early marker of cardiomyopathy progression. This method shows great potential for early detection and ongoing monitoring, which could enhance patient outcomes by enabling timely interventions and more effective disease management.

In the current study, segmental LGE distribution was most frequent in the inferolateral region, then in the anterolateral region. Florian et al. [27] reported that LGE was mostly basal inferolateral (90%) and basal anterolateral (60%). The research study of Xu et al. [28] showed that the most frequently involved segments, at basal and middle levels, were inferolateral and anterolateral. CMR imaging provides enhanced imaging clarity in DMD, particularly in male patients. Moreover, CMR enables the evaluation of myocardial strain through harmonic phase imaging (HARP) and CMR-FT. While HARP imaging necessitates additional tagged images, limiting its clinical feasibility, CMR-FT imaging can be feasible using clinically obtained SSFP images, thus enhancing its practicality in clinical settings. Consequently, CMR-FT strain imaging may provide more clinically applicable strain measurements. CMR-FT revealed myocardial strain alterations among DMD patients not identified by STE [24].

The results of the current study align with those in the literature and proved several hypotheses, confirming CMR as the gold standard for detecting and assessing the severity of cardiomyopathy in DMD patients. It is the technique of choice for myocardial tissue characterization by detecting fibrosis and precisely estimating cardiac volumes and functions in DMD patients. It also highlights that CMR-FT can detect alterations in the myocardium of individuals with DMD, even in the absence of late gadolinium enhancement. In addition, this study demonstrated that the myocardial global strain parameters correlated well with LV geometry. This correlation suggests that alterations in the LV geometry, such as changes in wall thickness or thickening, are closely associated with changes in myocardial strain. Consequently, assessing these strain parameters can provide valuable insights into the structural and functional state of the heart, particularly in the context of various cardiac conditions [29,30].

The current study has several limitations. Initially, the study was limited to a single center, leading to potentially biased case selection. Moreover, DMD is a rare disease that posed challenges to the study, notably in recruiting enough participants from a single center due to its rarity. This limitation may have impacted the prediction accuracy of our findings. Despite these limitations, the notable results and robustness of the present research prompt one to consider expanding the used dataset and exploring the application of artificial intelligence and machine learning in future research projects. In future research, leveraging deep learning algorithms holds great promise for aiding in the early detection of cardiac dysfunction in DMD patients and assessing progression rates to aid in therapy assessment.

5. Conclusions

In conclusion, the current study demonstrates that CMR-FT is an effective and leading technique for the early diagnosis of subclinical cardiomyopathy in pediatric patients with DMD. By detecting initial myocardial alterations without the need for gadolinium, CMR-FT offers a non-invasive biomarker for identifying early cardiac changes, including myocardial fibrosis and dilated cardiomyopathy. Moreover, it provides valuable potential as a performance metric for assessing therapy effectiveness and guiding early interventions. This highlights its crucial role in the early detection and management of DMD cardiomyopathy in children.