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Clinical Investigations: NERVES AND MUSCLE |

Cardiac and Sternocleidomastoid Muscle Involvement in Duchenne Muscular Dystrophy*: An MRI Study FREE TO VIEW

Sophie Mavrogeni, MD; George E. Tzelepis, MD, FCCP; George Athanasopoulos, MD; Themistoklis Maounis, MD; Marouso Douskou, MD; Antigoni Papavasiliou, MD; Dennis V. Cokkinos, MD
Author and Funding Information

*From the Onassis Cardiac Surgery Center (Drs. Mavrogeni, Athanasopoulos, Maounis, and Cokkinos), University of Athens Medical School (Dr. Tzelepis), Athens, Greece; and Bioiatriki MRI Unit (Dr. Douskou), Athens, Greece; and the Pentelis Children’s Hospital (Dr. Papavasiliou), Athens, Greece.

Correspondence to: Sophie Mavrogeni, MD, 50 Esperou St, 175–61 P.Faliro, Athens, Greece; e-mail: soma@aias.gr



Chest. 2005;127(1):143-148. doi:10.1378/chest.127.1.143
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Published online

Objective: To examine the extent of cardiac muscle and sternocleidomastoid muscle (SCM) involvement detected by MRI measurement of T2 relaxation time in patients with Duchenne muscular dystrophy (DMD) and no cardiorespiratory symptoms.

Design: Prospective controlled study.

Setting: Teaching referral hospital and university hospital.

Subjects: Seventeen patients with DMD (age range, 7 to 25 years) and 17 age-matched control subjects. All patients were free of cardiac or respiratory complaints and had normal ECG, echocardiograph, and Holter monitor examination findings.

Methods: We assessed respiratory function by means of standard pulmonary function testing. MRI measurements included the T2 relaxation time of the myocardium and the SCM in patients and control subjects.

Results: The FVC and FEV1 values were lower in patients with DMD than in age-matched control subjects, whereas the FEV1/FVC ratio was normal in all subjects. Patients with DMD had lower T2 relaxation time of the heart (37.8 ± 6.1 ms vs 58.1 ± 7.1 ms, p < 0.001) and lower T2 relaxation time of the right SCM (24.5 ± 2.6 ms vs 42.2 ± 1.3 ms, p < 0.001) and left SCM (23.2 ± 3.2 ms vs 42.2 ± 1.6 ms, p < 0.001), compared to control subjects (± SD). In children (< 12 years of age), the T2 of the SCM was lower than that of the control subjects, but T2 of the heart did not differ between the two groups. In the patient group, T2 relaxation time of the heart decreased with age (r = − 0.80, p < 0.001). In patients with FVC < 80% of predicted, the T2 values of the heart were lower than the T2 values of patients with FVC ≥ 80% of predicted (35.6 ± 5.8 ms vs 41.8 ± 4.6 ms, p < 0.05).

Conclusions: MRI measurements of the T2 relaxation time in the myocardium and SCM of patients with DMD and no cardiorespiratory symptoms are abnormal, indicating altered tissue composition. These measurements may prove a clinically useful test for monitoring cardiac and respiratory muscle involvement in these patients.

Figures in this Article

Duchenne muscular dystrophy (DMD) is a familial neuromuscular disorder with variable clinical manifestations in which mortality is primarily related to cardiac and/or respiratory muscle failure.1In these patients, cardiac and respiratory muscle dysfunction typically occurs several years after the onset of neuromuscular symptoms, and its occurrence depends on the patient surviving long enough to acquire symptomatic involvement.2

MRI has been proposed as a readily available, noninvasive method of monitoring tissue structure in these patients. Unlike other modalities, MRI does not use ionizing radiation, produces high-resolution images, and can be used for quantitative tissue characterization by measuring the T2 relaxation time of the muscles. In patients with DMD, the T2 relaxation time in peripheral muscles was significantly different from that measured in healthy control subjects,35 essentially reflecting differences in fat and water composition between diseased and healthy muscles. Because the T2 relaxation time changes as the disease progresses, it could be used to monitor disease progression and possibly response to therapy in these patients.3

To our knowledge, no previous study has applied a similar technique to quantify tissue composition in the heart and respiratory muscles of patients with DMD. Therefore, this study was undertaken with the objective to examine the extent to which MRI measurements of T2 relaxation time can detect differences in tissue composition between patients with DMD who had no clinical evidence of cardiorespiratory symptoms and age-matched healthy volunteers.

Seventeen male patients with DMD (age range, 7 to 25 years) and 17 age-matched male control subjects were included in the study. Five of the patients and five control subjects were children (age range, 7 to 12 years). The diagnosis of DMD was initially based on the characteristic clinical history and neuromuscular findings, and was supported by electromyography, muscular biopsy with special dystrophin immunostaining, and DNA testing. All patients were free of cardiac or respiratory complaints and had normal ECG, echocardiographic, and Holter monitor examination findings. None of the patients were receiving any medication. All subjects (or their parents) gave informed consent, and the study was approved by the hospital ethics committee.

Pulmonary function testing included measurement of spirometry according to standard methods (Masterlab; Jaeger; Wurzung, Germany). For all parameters, actual and percentage of predicted values are presented.6

MRI images were obtained with a whole-body superconducting magnet (GE-Vectra; General Electric; Milwaukee, WI) operating at 0.5 T; ECG-triggered images were acquired. Multiple coronal spin-echo planes from the cervical area were taken. The plane where both sternocleidomastoid muscles (SCMs) were adequately imaged was used for T2 relaxation time measurements. For the heart study, initially a coronal spin-echo scout plane was taken to identify the best heart image. Multiple horizontal, long-axis, spin-echo planes were taken using the scout image. The best horizontal long-axis image was used for T2 relaxation time measurements of the left ventricular myocardium. Myocardial muscle and SCM T2 relaxation time was calculated using four echo times (17 to 68 ms) and repetition time at least 2,000 ms, which is equal to two or three R-R intervals. The slice thickness was 10 mm with field of view of 45 cm; the image reconstruction axis was 224 × 160. Cardiac and respiratory muscle T2 relaxation time was measured using three regions of interest (ROIs) in each area. For the SCM area, the ROIs were selected in the center of the muscle, where the best signal was obtained. For the cardiac study, the ROIs were selected in the mid-ventricular septum, anterior and inferior wall.

Two independent readers, blinded to the patient or subject status, performed the image analysis. Assuming single exponential behavior of all tissues, cardiac and skeletal muscle pixel signal intensity decays exponentially with echo time in the base images of a multiecho sequence. The rate of exponential decay can thus be calculated by means of a mathematical fit on signal intensity and echo time data values. The intraobserver and interobserver coefficients of variation for T2 measurements were 7% and 13%, respectively.

Continuous variables were expressed as mean ± SD and compared by means of Mann-Whitney test. The correlation of variables was expressed as the Spearman correlation coefficient. Significance was accepted at a p value < 0.05.

Table 1 shows pulmonary function testing parameters in patients and age-matched control subjects. FVC and FEV1 values (both absolute and percentage of predicted) were lower in patients with DMD than in age-matched control subjects. Unlike the adults, children with DMD had FVC and FEV1 values similar to those of the age-matched control subjects. The FEV1/FVC ratio was normal in all subjects.

Figure 1 shows representative MRI images from which the data were derived in a patient with DMD. In comparison with the control group, DMD patients had lower T2 relaxation time values of the heart (37.8 ± 6.1 ms vs 58.1 ± 7.1 ms, p < 0.001) and lower T2 relaxation time values of both right and left SCMs, (right SCM, 24.5 ± 2.6 ms vs 42.2 ± 1.3 ms, p < 0.001; left SCM, 23.2 ± 3.2 ms vs 42.2 ± 1.6 ms, p < 0.001; Table 2 ).

On the basis of the FVC percentage of predicted, the patients were classified in two subgroups, one group (n = 6) with FVC equal or > 80% of predicted (range, 80.8 to 118.4%), and a second group (n = 11) with a FVC < 80% of predicted (range, 39.6 to 76.1%). Comparison of T2 values between these two subgroups showed that in those with FVC < 80% predicted, the heart T2 was lower than that of patients with FVC > 80% predicted (35.6 ± 5.8% vs 41.8 ± 4.6%, p < 0.05); there were no differences in the SCM T2 values for these two subgroups.

When data were analyzed in separate age groups, in the adult DMD patients T2 relaxation time of the heart and right and left SCM was significantly lower compared to control subjects (p < 0.001) [Table 2]. In the pediatric DMD patients ≤ 12 years old, T2 relaxation time of the heart was similar to that of pediatric control subjects, but T2 relaxation time of right and left SCMs was significantly lower compared to control subjects (p < 0.001) [Table 2].

In the entire group of patients, T2 relaxation time of the heart decreased with age (r = − 0.80, p < 0.001; Fig 2 ), while in the control population T2 relaxation increased with age (r = 0.90, p < 0.001). Moreover, in the patient population T2 relaxation time of the heart correlated with FVC percentage of predicted (r = 0.54, p < 0.05), but not with T2 relaxation time of left SCM or right SCM.

The T2 of the left SCM correlated with the T2 of the right SCM (r = 0.59, p < 0.01). The T2 of the left SCM, but not the right SCM, correlated negatively with age (r = − 0.48, p < 0.05). There was no correlation between FVC percentage of predicted and age, or between FVC percentage of predicted and T2 of the left SCM or T2 of the right SCM.

In a group of patients with DMD, with no cardiorespiratory symptoms, MRI measurements of T2 relaxation time in the myocardium and the SCM were lower than in age-matched control subjects. Unlike the T2 values in the healthy volunteers, in the patient group the older the patient the lower the myocardial T2 relaxation time.

DMD is a myopathy characterized by a defect in the p21 band of the X chromosome that is responsible for dystrophin, a protein located on the inner surface of the sarcolemma. In affected individuals, the absent or diminished dystrophin leads to progressive skeletal muscle failure.1

MRI provides noninvasive information on tissue structure. Using specifically designed sequences, the proton density and the relaxation times (T1 and T2) of the mobile proton can be measured.5,78 In patients with DMD, MRI and quantitative maps of relaxation times measured on peripheral muscles showed that these indexes were closely related to muscle function and indicated that they could be used to follow disease progression and potentially to provide an accurate measure of response to therapy.34,9

The cardiac involvement in DMD, which is characterized by cardiac muscle degeneration with fibrous tissue replacement and fatty infiltration, typically occurs late in the course of the disease.10 It is estimated that approximately 75% of patients with DMD die of respiratory failure and approximately 20% die of heart failure.1011 In a small percentage of patients, myocardial impairment may progress more quickly than skeletal muscle impairment and may lead to heart failure and death in relatively short period of time.10

In an effort to detect early myocardial disease, previous studies used specific tests of myocardial function including 201Tl scintigraphy, echocardiography, and systolic time intervals or various ECG indexes. Kawai et al12found no significant relationship between the presence of perfusion defects in thallium scintigraphy and the skeletal muscle involvement. Similarly, echocardiographic measurements of ventricular wall growth or shortening fraction were inadequate to track the degenerative cardiac process in the study by Goldberg et al.13In a group of patients with myotonic dystrophy and no clinical signs of heart disease, Venco et al14found only minor abnormalities of left ventricular function by echocardiography, which bore no relationship with skeletal muscle involvement. In a group of patients with DMD studied by Corrado and coworkers15left ventricular dysfunction per se, defined by echocardiography as decreased ejection fraction and fractional shortening, could provide some prognostic value regarding mortality. However, the ejection fraction lacked prognosticating ability during a period of approximately 5 years after echocardiographic assessment, the survival curves of patients with and without depressed ventricular function being identical. In another study, Backman and Nylander16 prospectively studied patients with DMD by using several noninvasive tests, including echocardiography, systolic time intervals, ECG parameters, as well as spirometry and indexes of skeletal muscle function. They found no useful relationship between the various noninvasive parameters and skeletal muscle tests or lung function tests. More recently Giglio et al17 found that ultrasound tissue characterization can detect preclinical myocardial structural changes in children with DMD, but at the moment there are no follow-up studies to assess the importance of this finding in the prediction of the onset of overt cardiomyopathy.

This is the first MRI study to detect myocardial abnormalities in patients with DMD using commercially available systems. Although our study included patients with normal ejection fraction and no clinical evidence of cardiac disease, the majority of patients had abnormal T2 values. The abnormal T2 relaxation time and its negative relationship with age suggest that cardiac involvement may occur relatively early in the disease and may progress with age. In the subgroup of patients who were < 12 years old, the T2 values did not differ from those found in age-matched normal control subjects. The explanation for this finding may be twofold. The normal T2 in this group of children may indicate that the myocardial changes were too small to be detected by MRI or alternatively myocardial involvement occurs after that age. Our findings are in agreement with those by Crilley at al,18 who used magnetic resonance spectroscopy to measure the ratio of cardiac phosphocreatine to adenosine in patients with Becker muscular dystrophy and carriers with DMD. Their finding of reduced cardiac phosphocreatine to adenosine ratios in both patient cohorts in the absence of left ventricular dysfunction as assessed by echocardiography suggests that cardiac metabolic dysfunction precedes the deterioration of clinical function.

Given the inherent inability of MRI to depict diaphragmatic muscle,19 we measured sternocleidomastoid T2 relaxation time rather than diaphragmatic T2 time. The low SCM T2 values indicate that these muscles are also involved in patients with no respiratory complaints, and that the process appears to precede that of the myocardial process. The finding that of the two T2 SCM values only the T2 of the left SCM correlated with age may indicate that the disease may be heterogeneous and asymmetrical, as in some peripheral muscles4 or, alternatively, the onset and progression of the degenerative process may vary among patients.

As in the case of cardiomyopathy, the degree of respiratory muscle involvement in DMD cannot be reliably assessed, at least in the early stages, by measuring FVC or respiratory muscle strength.2021 In our study, the lack of correlation between FVC (percentage of predicted) and age is in agreement with previous reports22 of significant variability in the evolution of the pulmonary function in patients with DMD. In other studies2223 only very low FVC values (< 1 L) were associated with prognostic information about survival. However, the rate of decline of FVC was an independent predictor of life expectancy and was significantly less in patients dying after the age of 21 years22; and, according to these authors, serial measurements of FVC provide a simple and reliable means of assessing disease progression in DMD. The limited ability of conventional pulmonary function parameters to predict respiratory mortality in these patients may in part be due to several reasons. First, these specific tests of pulmonary function measure the net result of two simultaneously occurring and opposing processes on the respiratory system, the growth (of both lungs and respiratory muscles) and the degenerative process. Depending on the patient’s age and stage of degenerative process, the FVC changes over time may follow a specific pattern characterized by an ascending, plateau, and descending phase.21 Furthermore, in many patients FVC may be additionally affected by the chest wall stiffness related to spinal deformity, or by inaccurate measuring techniques if arm span is used as substitute for height in wheelchair-bound individuals with upper-extremity contractures.23 To the extent that the T2 relaxation time of the rib cage muscles accurately assesses muscle composition and particularly changes over time, it may be a better predictor of respiratory muscle involvement in DMD.

Certain limitations of the study should be considered. First, this is a cross-sectional study in a small cohort of patients with DMD. Our data need to be duplicated in a larger group of patients, in whom involvement of cardiac and respiratory muscles should also include a longitudinal MRI assessment. In addition, assessment of the diaphragm, rather than the SCM, by MRI might provide a better assessment of the respiratory muscle involvement in these patients.

In conclusion, in a group of patients with DMD and no cardiorespiratory symptoms, we found that the MRI measurements of the T2 relaxation times of the cardiac muscle and SCM were decreased in comparison with healthy volunteers matched for age. Further work is needed to study the role of these indexes in reliably tracking the myopathic process and providing clinically useful information about the dysfunction of both the heart and the respiratory muscles in patients with DMD.

Abbreviations: DMD = Duchenne muscular dystrophy; ROI = region of interest; SCM = sternocleidomastoid muscle

Table Graphic Jump Location
Table 1. Pulmonary Function Testing Parameters in Patients With DMD and Healthy Control Subjects*
* 

Data are presented as mean ± SD.

 

p < 0.001.

 

p < 0.01.

§ 

p < 0.05.

Figure Jump LinkFigure 1. MRI of the heart muscle (top) and the SCM (bottom) in a patient with DMD.Grahic Jump Location
Table Graphic Jump Location
Table 2. T2 Relaxation Time Values of the Heart and SCM (Right and Left) in Patients With DMD and Control Subjects*
* 

Data are presented as mean ± SD.

 

p < 0.001.

Figure Jump LinkFigure 2. Relationship of the myocardial T2 relaxation time and age in patients with DMD (top) and healthy control subjects (bottom). Note that T2 decreases with age in the patients with DMD and increases with age in the healthy control subjects.Grahic Jump Location
Emery, AE (2002) The muscular dystrophies.Lancet359,687-695. [CrossRef] [PubMed]
 
Smith, PEM, Calverley, PMA, Edwards, RHT, et al Practical considerations of respiratory care of patients with muscular dystrophy.N Engl J Med1987;316,1197-1205. [CrossRef] [PubMed]
 
Huang, Y, Majumdar, S, Genant, HK, et al Quantitative MR relaxometry study of muscle composition and function in Duchenne muscular dystrophy.J Magn Reson Imaging1994;4,59-64. [CrossRef] [PubMed]
 
Phoenix, J, Betal, D, Roberts, N, et al Objective quantification of muscle and fat in human dystrophic muscle by magnetic resonance image analysis.Muscle Nerve1996;19,302-310. [CrossRef] [PubMed]
 
Dunn, JF, Zaim-Wadghiri, Y Quantitative magnetic resonance imaging of the mdx mouse model of Duchenne muscular dystrophy.Muscle Nerve1999;22,1367-1371. [CrossRef] [PubMed]
 
Quanjer, P, Tammeling, G, Cotes, Y, et al Lung volumes and forced ventilatory flows.Eur Respir J1993;6,5-40. [PubMed]
 
Misra, LK, Luthra, MG, Amtey, SR, et al Enhanced T1 differentiation between normal and dystrophic muscle.Magn Reson Imaging1984;2,33-35. [CrossRef] [PubMed]
 
Narayana, PA, Brey, WW, Kulkarni, MV, et al In vivoproton spin-lattice relaxation times of normal and dystrophic muscles.Magn Reson Imaging1987;4,153-161
 
Matsumura, K, Nakano, I, Fukuda, N, et al Proton spin-lattice relaxation time of Duchenne dystrophy skeletal muscle by magnetic resonance imaging.Muscle Nerve1988;11,97-102. [CrossRef] [PubMed]
 
Sasaki, K, Sakata, K, Kachi, E, et al Sequential changes in cardiac structure and function in patients with Duchenne type muscular dystrophy: a two-dimensional echocardiographic study.Am Heart J1998;135,937-944. [CrossRef] [PubMed]
 
Perloff, JK, Leon, AC, O’Doherty, D The cardiomyopathy of progressive muscular dystrophy.Circulation1966;11,625-648
 
Kawai, N, Sotobata, I, Okada, M, et al Evaluation of myocardial involvement in Duchenne’s progressive muscular dystrophy with thallium-201 myocardial perfusion imaging.Jpn Heart J1985;26,767-775. [CrossRef] [PubMed]
 
Goldberg, SJ, Stern, LZ, Feldman, L, et al Serial left ventricular wall measurements in Duchenne’s muscular dystrophy.J Am Coll Cardiol1983;2,136-142. [CrossRef] [PubMed]
 
Venco, A, Saviotti, M, Besana, D, et al Noninvasive assessment of left ventricular function in myotonic muscular dystrophy.Br Heart J1978;40,1262-1266. [CrossRef] [PubMed]
 
Corrado, G, Lissoni, A, Beretta, S, et al Prognostic value of electrocardiograms, ventricular late potentials, ventricular arrhythmias, and left ventricular systolic dysfunction in patients with Duchenne muscular dystrophy.Am J Cardiol2002;89,838-841. [CrossRef] [PubMed]
 
Backman, E, Nylander, E The heart in Duchenne muscular dystrophy: a non-invasive longitudinal study.Eur Heart J1992;13,1239-1244. [PubMed]
 
Giglio, V, Pasceri, V, Messano, L, et al Ultrasound tissue characterization detects preclinical myocardial structural changes in children affected by Duchenne muscular dystrophy.J Am Coll Cardiol2003;42,309-316. [CrossRef] [PubMed]
 
Crilley, JG, Boehm, EA, Rajagopolan, B, et al Magnetic resonance spectroscopy evidence of abnormal cardiac energetics in Xp21 muscular dystrophy.J Am Coll Cardiol2000;36,1953-1958. [CrossRef] [PubMed]
 
Gierada, DS, Curtin, JJ, Erickson, SJ, et al Fast gradient echo magnetic resonance imaging of the normal diaphragm.J Thorac Imaging1997;12,70-74. [CrossRef] [PubMed]
 
Hahn, A, Bach, JR, Renardel-Irani, A, et al Clinical implications of maximal respiratory pressure determinations for individuals with Duchenne muscular dystrophy.Arch Phys Med Rehabil1997;78,1-6. [CrossRef] [PubMed]
 
Rideau, Y, Jamkowsi, LW, Grellet, J Respiratory function in the muscular dystrophies.Muscle Nerve1981;4,155-164. [CrossRef] [PubMed]
 
Phillips, MF, Quinlivan, RC, Edwards, RH, et al Changes in spirometry over time as a prognostic marker in patients with Duchenne muscular dystrophy.Am J Respir Crit Care Med2001;164,2191-2194. [PubMed]
 
Lyager, S, Steffensen, B, Juhl, B Indicators of need for mechanical ventilation in Duchenne muscular dystrophy and spinal muscular atrophy.Chest1995;108,779-785. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1. MRI of the heart muscle (top) and the SCM (bottom) in a patient with DMD.Grahic Jump Location
Figure Jump LinkFigure 2. Relationship of the myocardial T2 relaxation time and age in patients with DMD (top) and healthy control subjects (bottom). Note that T2 decreases with age in the patients with DMD and increases with age in the healthy control subjects.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Pulmonary Function Testing Parameters in Patients With DMD and Healthy Control Subjects*
* 

Data are presented as mean ± SD.

 

p < 0.001.

 

p < 0.01.

§ 

p < 0.05.

Table Graphic Jump Location
Table 2. T2 Relaxation Time Values of the Heart and SCM (Right and Left) in Patients With DMD and Control Subjects*
* 

Data are presented as mean ± SD.

 

p < 0.001.

References

Emery, AE (2002) The muscular dystrophies.Lancet359,687-695. [CrossRef] [PubMed]
 
Smith, PEM, Calverley, PMA, Edwards, RHT, et al Practical considerations of respiratory care of patients with muscular dystrophy.N Engl J Med1987;316,1197-1205. [CrossRef] [PubMed]
 
Huang, Y, Majumdar, S, Genant, HK, et al Quantitative MR relaxometry study of muscle composition and function in Duchenne muscular dystrophy.J Magn Reson Imaging1994;4,59-64. [CrossRef] [PubMed]
 
Phoenix, J, Betal, D, Roberts, N, et al Objective quantification of muscle and fat in human dystrophic muscle by magnetic resonance image analysis.Muscle Nerve1996;19,302-310. [CrossRef] [PubMed]
 
Dunn, JF, Zaim-Wadghiri, Y Quantitative magnetic resonance imaging of the mdx mouse model of Duchenne muscular dystrophy.Muscle Nerve1999;22,1367-1371. [CrossRef] [PubMed]
 
Quanjer, P, Tammeling, G, Cotes, Y, et al Lung volumes and forced ventilatory flows.Eur Respir J1993;6,5-40. [PubMed]
 
Misra, LK, Luthra, MG, Amtey, SR, et al Enhanced T1 differentiation between normal and dystrophic muscle.Magn Reson Imaging1984;2,33-35. [CrossRef] [PubMed]
 
Narayana, PA, Brey, WW, Kulkarni, MV, et al In vivoproton spin-lattice relaxation times of normal and dystrophic muscles.Magn Reson Imaging1987;4,153-161
 
Matsumura, K, Nakano, I, Fukuda, N, et al Proton spin-lattice relaxation time of Duchenne dystrophy skeletal muscle by magnetic resonance imaging.Muscle Nerve1988;11,97-102. [CrossRef] [PubMed]
 
Sasaki, K, Sakata, K, Kachi, E, et al Sequential changes in cardiac structure and function in patients with Duchenne type muscular dystrophy: a two-dimensional echocardiographic study.Am Heart J1998;135,937-944. [CrossRef] [PubMed]
 
Perloff, JK, Leon, AC, O’Doherty, D The cardiomyopathy of progressive muscular dystrophy.Circulation1966;11,625-648
 
Kawai, N, Sotobata, I, Okada, M, et al Evaluation of myocardial involvement in Duchenne’s progressive muscular dystrophy with thallium-201 myocardial perfusion imaging.Jpn Heart J1985;26,767-775. [CrossRef] [PubMed]
 
Goldberg, SJ, Stern, LZ, Feldman, L, et al Serial left ventricular wall measurements in Duchenne’s muscular dystrophy.J Am Coll Cardiol1983;2,136-142. [CrossRef] [PubMed]
 
Venco, A, Saviotti, M, Besana, D, et al Noninvasive assessment of left ventricular function in myotonic muscular dystrophy.Br Heart J1978;40,1262-1266. [CrossRef] [PubMed]
 
Corrado, G, Lissoni, A, Beretta, S, et al Prognostic value of electrocardiograms, ventricular late potentials, ventricular arrhythmias, and left ventricular systolic dysfunction in patients with Duchenne muscular dystrophy.Am J Cardiol2002;89,838-841. [CrossRef] [PubMed]
 
Backman, E, Nylander, E The heart in Duchenne muscular dystrophy: a non-invasive longitudinal study.Eur Heart J1992;13,1239-1244. [PubMed]
 
Giglio, V, Pasceri, V, Messano, L, et al Ultrasound tissue characterization detects preclinical myocardial structural changes in children affected by Duchenne muscular dystrophy.J Am Coll Cardiol2003;42,309-316. [CrossRef] [PubMed]
 
Crilley, JG, Boehm, EA, Rajagopolan, B, et al Magnetic resonance spectroscopy evidence of abnormal cardiac energetics in Xp21 muscular dystrophy.J Am Coll Cardiol2000;36,1953-1958. [CrossRef] [PubMed]
 
Gierada, DS, Curtin, JJ, Erickson, SJ, et al Fast gradient echo magnetic resonance imaging of the normal diaphragm.J Thorac Imaging1997;12,70-74. [CrossRef] [PubMed]
 
Hahn, A, Bach, JR, Renardel-Irani, A, et al Clinical implications of maximal respiratory pressure determinations for individuals with Duchenne muscular dystrophy.Arch Phys Med Rehabil1997;78,1-6. [CrossRef] [PubMed]
 
Rideau, Y, Jamkowsi, LW, Grellet, J Respiratory function in the muscular dystrophies.Muscle Nerve1981;4,155-164. [CrossRef] [PubMed]
 
Phillips, MF, Quinlivan, RC, Edwards, RH, et al Changes in spirometry over time as a prognostic marker in patients with Duchenne muscular dystrophy.Am J Respir Crit Care Med2001;164,2191-2194. [PubMed]
 
Lyager, S, Steffensen, B, Juhl, B Indicators of need for mechanical ventilation in Duchenne muscular dystrophy and spinal muscular atrophy.Chest1995;108,779-785. [CrossRef] [PubMed]
 
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