CLINICAL RESEARCH
Circumferential Strain Analysis Identifies Strata of Cardiomyopathy in Duchenne Muscular DystrophyA Cardiac Magnetic Resonance Tagging Study
Kan N. Hor, MD*,
Janaka Wansapura, PhD ,
Larry W. Markham, MD ,
Wojciech Mazur, MD ,
Linda H. Cripe, MD*,
Robert Fleck, MD,
D. Woodrow Benson, MD, PhD* and
William M. Gottliebson, MD*,*
* Department of Cardiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
Department of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
Department of Pediatric Cardiology, Vanderbilt University, Nashville, Tennessee
Christ Hospital, Cincinnati, Ohio
Manuscript received June 17, 2008;
revised manuscript received October 31, 2008,
accepted December 18, 2008.
* Reprint requests and correspondence: Dr. William M. Gottliebson, Cincinnati Children's Hospital Medical Center, Division of Cardiology, 3333 Burnet Avenue, Cincinnati, Ohio 45229-3039 (Email: bill.gottliebson{at}cchmc.org).
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Abstract
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Objectives: This study sought to evaluate the natural history of occult cardiac dysfunction in Duchenne muscular dystrophy (DMD).
Background: Duchenne muscular dystrophy is characterized by progressive cardiac dysfunction and myocardial fibrosis late in the disease process. We hypothesized that left ventricular myocardial peak circumferential strain ( cc) would decrease in DMD before global systolic functional abnormalities regardless of age or ventricular ejection fraction (EF).
Methods: We evaluated cardiac magnetic resonance image (MRI) data from 70 DMD patients and 16 aged-matched control subjects. Standard imaging data included steady-state free precession short-axis cine stack images, cine myocardial tagged images, and myocardial delayed enhancement (MDE) (an indicator of myocardial fibrosis) sequences. Analysis was performed with QMASS (Medis Medical Imaging Systems, Leiden, the Netherlands) and HARP (Diagnosoft, Palo Alto, California) software. The DMD patient data were subdivided by age (<10 or >10 years), EF (>55% or <55%), and the presence or absence of MDE.
Results: The DMD patients with normal EF had reduced cc at an early age (<10 years) compared with control subjects (p < 0.01). The DMD patients age >10 years with normal EF had further decline in cc compared with younger DMD patients (p < 0.01). There was further decline in cc with age in patients with reduced EF (p < 0.01) without MDE. The oldest patients, with both reduced EF and positive MDE, exhibited the lowest cc. None of the patients had ventricular hypertrophy.
Conclusions: Myocardial strain abnormalities are prevalent in young DMD patients despite normal EF, and these strain values continue to decline with advancing age. Strain analysis in combination with standard MRI and MDE imaging provides a means to stratify DMD cardiomyopathy.
Key Words: cardiac magnetic resonance imaging • circumferential strain • Duchenne muscular dystrophy
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Abbreviations and Acronyms
| | DMD = Duchenne muscular dystrophy | | ECG = electrocardiogram | | cc
= circumferential strain | | EF = ejection fraction | | MDE = myocardial delayed enhancement | | MRI = magnetic resonance imaging/image | | SSFP = steady-state free precession | | TTE = transthoracic echocardiogram |
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Duchenne muscular dystrophy (DMD), an X-linked recessive disorder affecting approximately 1 in 3,500 male subjects (1), results from a mutation in the gene that encodes dystrophin, a sarcolemmal protein abundant in skeletal and cardiac muscle cells (1). DMD is characterized by progressive skeletal muscle weakness, with loss of ambulation between the ages of 7 and 13 years. Death secondary to cardiac or respiratory failure typically occurs in the second or third decade. Cardiac disease manifests as a dilated cardiomyopathy (2,3). End-stage cardiac pathology consists of alternating areas of myocyte hypertrophy, atrophy, and fibrosis (3,4).
Use of corticosteroids and supportive respiratory care (5–7) have improved outcomes in DMD patients such that cardiomyopathy is now the leading cause of death (8). The progression of cardiomyopathy does not correlate to the severity of skeletal muscle weakness, and early manifestations of heart failure in DMD patients often go unrecognized due to lack of classic signs and symptoms (9). Previous investigators have demonstrated that cardiac disease is underway long before symptoms appear (10–12).
Traditionally, assessment of global cardiac function has been evaluated via transthoracic echocardiography (TTE) (2,13,14). However, this modality has proved challenging in the DMD population. TTE rarely detects functional abnormalities during the first decade (15), and acoustic windows in DMD patients tend to be limited due to altered body habitus, including scoliosis and significant chest wall adiposity. To overcome these limitations, our center and others have turned to cardiac magnetic resonance imaging (MRI) for primary screening of global cardiac function in DMD patients (16–18). Recent reports have shown that occult cardiac dysfunction (19) and myocardial fibrosis (16) can be diagnosed by MRI in DMD patients. However, the natural history of the cardiac dysfunction, manifest as reduction in peak left ventricular myocardial circumferential strain (cc), has not been reported. We hypothesized that abnormalities of cc would exist early in the course of DMD cardiomyopathy despite normal ejection fraction (EF) and would be progressive during the course of the disease, as cardiac dysfunction becomes more generalized.
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Methods
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Study population.
Data were analyzed from records of DMD patients followed at Cincinnati Children's Hospital Medical Center. The diagnosis of DMD was confirmed by a skeletal muscle biopsy showing absent dystrophin and/or deoxyribonucleic acid analysis demonstrating a characteristic dystrophin mutation in all patients.
MRI inclusion and exclusion criteria.
The DMD patients who underwent clinical MRI studies between September 2005 and September 2007 were included in this analysis. Only quality tagged cine MRIs were included for analysis (confirmed by 3 independent expert readers: R.J.F., W.M.G., and K.N.H.). An age-matched control group underwent an identical protocol. All subjects (control subjects and DMD patients) were >5 years of age, thereby eliminating the need for sedation. The MRI studies were performed on 97 DMD patients between September 2005 and September 2007. Data from 27 of 97 patients was excluded due to absence of tagged images (n = 18) or poor tag quality secondary to breathing artifact or patient movement (n = 9). The Institutional Review Board at the Cincinnati Children's Hospital Medical Center approved the study.
Subject stratification.
The subject data were stratified into 5 groups: Group A (control subjects) and Groups B to E (DMD patients), grouped according to age, EF, and the presence of myocardial fibrosis on the basis of positive myocardial delayed enhancement (MDE) imaging (Fig. 1). Because prior studies have rarely identified cardiac dysfunction before age 10 years (15), we stratified DMD patients  10 or >10 years. As such, Group B comprised DMD patients age <10 years with normal EF and negative MDE. Because MDE has usually been associated with advanced cardiac disease, patients >10 years were further stratified by MDE status (i.e., with or without MDE). Lastly, we stratified the patients age >10 years without MDE into those with normal EF and those with reduced EF. Thus, Group C comprised DMD patients age >10 years with normal EF and negative MDE. Group D comprised DMD patients age >10 years with reduced EF (<55%) but negative MDE. Finally, Group E patients comprised DMD patients age >10 years with reduced EF and positive MDE.
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Figure 1 Group Stratification
Stratification of Duchenne muscular dystrophy (DMD) patients is based on age, ejection fraction (EF), and presence or absence of myocardial delayed enhancement (MDE).
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MRI acquisition.
The MRI studies were conducted either on a Siemens 3-T Trio (Siemens Medical Solutions, Malvern, Pennsylvania/Erlangen, Germany) or on a 1.5-T GE Signa Excite (GE Healthcare, Milwaukee, Wisconsin). The type of machine used on the DMD patients and control subjects was based solely on clinical availability, independent of the patient's clinical status.
Imaging protocols.
Ventricular Volumetry and Global Functional Imaging
Cardiac functional imaging was performed with retrospective electrocardiogram (ECG)-gating, segmented steady-state free precession (SSFP) technique after localized shimming and/or frequency adjusting. Subjects were breath-held as tolerated; for those subjects who could not adequately breath-hold, a free breathing technique with multiple signal averaging was used. Standard imaging included a short-axis stack of cine SSFP images from cardiac base to apex; the short axis was prescribed as the perpendicular plane to the left ventricular long axis in 2- and 4-chamber views as previously described (20,21). Typical scan parameters included field of view 32 to 38 cm, slice thickness 5 to 6 mm, gap 1 to 2 mm, number of excitations 2 (breath hold; 4 to 5 for free breathing), echo time/repetition time (TE/TR) 1.4/2.8 (Siemens Medical Solutions), TE/TR 2.0/4.0 (GE Healthcare), and in-plane resolution 1.2 to 2.2 mm. A minimum of 12 slices were performed, with 20 phases/slice. The typical temporal resolution of the cine SSFP images was 30 to 40 ms and was adjusted according to the patient's heart rate and ability to breath-hold. The radiofrequency flip angles were set between 50° and 70°, dependent on the patient's weight and height and the specific absorption rate level.
Myocardial Strain Imaging
Tagged cine MRIs were acquired in the short axis of the midventricle at the level of the papillary muscles (Fig. 2) with an ECG-triggered segmented k-space fast gradient echo sequence with spatial modulation of magnetization in orthogonal planes. Tag imaging was performed before administration of gadolinium. Grid tag spacing was 7 to 8 mm. The scan parameters used were: field of view (30 – 32) x (25 – 26) cm2, slice thickness 6 mm, flip angle 20°, TE/TR 3 ms/6.6 ms (GE Healthcare), TE/TR 3 ms/4.2 ms (Siemens Medical Solutions), views/segment 8 (GE Healthcare), views/segment 7 to 9 (Siemens Medical Solutions).
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Figure 2 Cardiac Magnetic Resonance Image
From the early systolic 4-chamber view (left), the short-axis of the midventricle is obtained at the level of the papillary muscles with a tag sequence (middle). Mesh overlaying of the tag image with a harmonic phase (HARP) software (Diagnosoft, Inc.) is shown (right).
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MDE
MDE imaging was performed on DMD patients when intravenous access was obtained (n = 54); no MDE imaging was performed in the control group. MDE imaging was performed via a FLASH inversion sequence recovery protocol 10 min after 0.2 mmol/kg gadolinium diethylenetriamine penta-acetic acid (Gd-DTPA) injection (16,22,23). MDE imaging was considered positive if any area of the mid-myocardium showed hyperenhancement (Fig. 3) as assessed by 3 independent expert observers (R.J.F., W.M.G., and K.N.H.) (24).
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Figure 3 MDE, an MRI Marker of Myocardial Fibrosis
Myocardial delayed enhancement (MDE) in the short-axis (A) and long-axis (B) planes indicates myocardial fibrosis in a 20-year-old Duchenne muscular dystrophy patient, as shown by the white arrows.
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Data analysis: ventricular volumetry, global functional data, and MDE status.
Ventricular volumes, mass, and global function were assessed via standard planimetry techniques with semi-automated computer software (QMASS version 6.1.5, Medis Medical Imaging Systems, Leiden, the Netherlands) by expert readers (R.J.F., W.M.G., and K.N.H.) (25,26). This assessment was performed on DICOM images from either scanner, independent of vendor or field strength (27,28). MDE status, ventricular volumes, mass, and EF were tabulated for each subject and then exported to a spreadsheet file.
Myocardial strain analysis.
Tagged images were analyzed with the HARmonic Phase (HARP, Diagnosoft, Palo Alto, California) technique (19,29–33). Only the midventricular slice was analyzed, on the basis of our experience and others (19) of limited reproducibility of the basal and apical slices. Details of cc analysis are described in the Online Appendix. The cc data were exported to a spreadsheet file for analysis. An average of all the regional values/subject was calculated as a composite regional strain value, to allow for comparison purposes (19,30–32,34). The average cc values for all subjects were then tabulated and grouped according to the group stratification criteria (see the Methods section) (Fig. 1). All HARP strain analyses were performed by an expert reader (K.N.H.). To assess interobserver variability of HARP strain analyses, a second expert reader (W.M.G.) performed the same analysis on subsets of patient (n = 10) and control (n = 5) data.
Statistical analyses.
All statistical analyses were performed with SPSS software version 16 (SPSS Inc., Chicago, Illinois). Differences in the means between the groups for all parametric data were assessed by analysis of variance. Due to unequal variance, post-hoc analysis was performed with the Games-Howell procedure to determine significance. For nonparametric data, the Mann-Whitney U test was performed. Probability values of <0.05 were considered statistically significant.
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Results
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Study population.
Data from 70 DMD patients (age 7 to 26 years) and 16 control subjects (age 6 to 34 years) were included in the study. The MDE sequence imaging was performed in 54 of 70 DMD patients; MDE imaging was not performed in 16 of 70 patients (9 from Group B, 5 from Group C, and 2 from Group D) lacking intravenous access. Patient stratification (Fig. 1) revealed the following: Group A (control subjects, n = 16); Group B (DMD patients age 10 years, n = 16), Group C (DMD patients age >10 years with normal EF, n = 31), Group D (DMD patients age >10 years with low EF but no MDE, n = 12), and Group E (DMD patients age >10 years with low EF and positive MDE, n = 11). Demographic data of the DMD and control groups were not significantly different (Table 1). The ECG findings of relative tachycardia were found in DMD patients, consistent with prior publications (35). None of the patients had ventricular hypertrophy, as evidenced by a normal mass–volume ratio and normal wall thicknesses (Online Table 1).
Circumferential strain values.
Control Subject Strain Data
All Group A subjects had cc <–16% and normal EF (Figs. 4
and 5B). Given the wide range of age and mean heart rate of control subjects, we performed an analysis of the effect of heart rate on cc. We divided control subjects into age 10 years (n = 7, mean age = 8 ± 1.3 years) or age >10 years (n = 9, mean age = 19.6 ± 8 years). There was no significant difference in cc (–19.3% vs. –18.2%, p = NS) or EF (66.3% vs. 64.2%, p = NS) between the subgroups, despite significant differences in heart rate between the groups (90 beats/min vs. 75 beats/min, p = 0.03).
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Figure 4 Box Plot of EF/Strata
Normal EF is seen in control subjects (Group A) and also in DMD patients (Groups B and C). Progressive decline in EF is seen in older patients (Group D), with further decline once MDE is present (Group E). Abbreviations as in Figure 1.
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DMD Patient Strain Data
No DMD patient had cc <–16%, even in the youngest DMD patients (Group B) with normal EF. Compared with the control subjects, 2 DMD groups (Group B and C) had similar EF (65.5% vs. 64.1%, p = NS) (Figs. 4 and 5B, Table 1). However, despite the similarity of EF, cc was significantly decreased in both Group B (–14.4% vs. –18.6%, p < 0.001) and Group C (–12.4% vs. –14.4%, p < 0.001) compared with the control group. Furthermore, the presence of reduced EF (47.4%, Group D) was associated with a further reduction in cc (–10% vs. –12.4%, p < 0.001) compared with the age-matched DMD cohort with normal EF (64.1%, Group C). The presence of overt ventricular dysfunction (EF = 32.7%) and MDE (Group E) was associated with significantly decreased cc compared with Group D (–6.5% vs. –10%, p < 0.0001) (Figs. 4 and 5A).
Variability of HARP strain measurements.
Two independent observers (W.M.G., K.N.H.) blindly performed separate quantitative strain analyses of myocardial cine MR-tagging images in 10 DMD patients and 5 control subjects. As previously shown (36), interobserver variability was low, with a mean difference of 0.009%.
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Discussion
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A major finding of this study is the detection of abnormal cc in young (age <10 years, Group B) DMD patients despite normal EF. There was further reduction in cc in older DMD patients with normal EF (Group C), a finding similar to that previously reported by Ashford et al. (19) in a cohort of DMD patients similar in mean age to Group C. It is important to note that the mean age of Groups B and C differs by almost 5 years, again placing emphasis on the young age at which reduced strain can be observed. In addition, with advancing age and reduced EF, there was further reduction in cc. A relationship between strain reduction and disease severity was further exemplified when MDE, the MRI marker of myocardial fibrosis, was considered. Taken together, we concluded that cc might be of value in defining the natural history of cardiac dysfunction in DMD and be a useful marker to assess therapeutic efficacy in young patients with normal global cardiac function.
It is not surprising to find abnormal cc in relatively young DMD boys. Duchenne muscular dystrophy results from a mutation in dystrophin, a large cytoskeletal protein localized to the inner surface of the sarcolemma membrane (1). Dystrophin mutation results in greatly reduced or absent dystrophin leading to a weakened sarcolemma that is more easily damaged during muscle contraction. A long-standing hypothesis regarding DMD disease pathogenesis is that loss of membrane integrity is a primary event leading to degeneration of myocytes. Intermittent tears in the cell membrane permit influx of calcium that then functions as a primary inducer of a destructive cascade culminating in myocyte necrosis and replacement fibrosis (37–39). Recent observations that the angiotensin II receptor blocker losartan reduces fibrotic disease in the mdx mouse implicate involvement of the transforming growth factor beta-1 and angiotensin II effector pathways in DMD pathogenesis (40). Collectively, these processes lead to necrosis, inflammation, and fibrosis manifested clinically by a progressive cardiac dysfunction (37,38,40,41). Because these processes are ongoing even in early stages of disease, abnormal cc should be expected.
There has long been interest in identification of early indicators of abnormal cardiac function in the DMD population. However, TTE evidence of cardiac dysfunction is not evident until late in the disease course (2,3,13,14,41,42). Studies using tissue Doppler imaging and strain rate imaging might detect early alteration in systolic and/or diastolic function compared with conventional imaging indexes such as EF and ventricular dimensions in DMD boys. In addition, TTE-based ultrasonic tissue characterization has been advocated as a means to characterize preclinical myocardial changes in DMD patients via integrated backscatter indexes (10,43). Although ultrasonic tissue characterization might prove to be useful for myocardial assessment, it too is limited by acoustic windows and angle dependence (10,43–45).
Study limitations.
Although significant differences in cc were demonstrated between young DMD patients with normal EF and older patients with reduced EF, this is a cross-sectional and not a serial study. Accordingly, repeat serial examinations would provide a more robust analysis of longitudinal cc in this patient population. In the current study, only the midventricular slice was analyzed secondary to our experience of limited reproducibility of the basal and apical slices. Studies were performed with 2 different vendors and magnetic field strengths, but we do not believe this confounds our data (27). Further MDE imaging was not performed in some younger patients with normal EF or in any of the control subjects. In our experience, MDE occurs late in the course of the disease, so it can reasonably be expected to have been absent in those individuals. Lastly, due to the size of our study population, we were not able to stratify cc on the basis of dystrophin genotype; such stratification might require multicenter studies. Despite these limitations, we propose that using cc determined by HARP analysis seems to be a sensitive indicator of cardiac dysfunction in DMD patients.
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Conclusions
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The MRI strain analysis in DMD patients demonstrates occult cardiovascular dysfunction in the presence of normal global function. The occult dysfunction progresses to global dysfunction with advancing age. Detection of such strain abnormalities might allow a better definition of the natural history of DMD cardiac dysfunction and also might provide a useful surrogate index to assess therapeutic efficacy.
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Appendix
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For a supplementary table and Methods section, please see the online version of this article.
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Acknowledgments
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The authors wish to recognize additional members of the Cincinnati Children's Hospital Medical Center MRI Team: Eric Crotty, MD, Kathy Helton, MD, and Amy Tipton, BFA, for clinical data acquisition and analysis.
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Footnotes
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This work was supported in part by the Children's Heart Association of Cincinnati (to Dr. Gottliebson) and the National Institutes of Health grant HL069712 (to Dr. Benson), Bethesda, Maryland.
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K. N. Hor, W. M. Gottliebson, C. Carson, E. Wash, J. Cnota, R. Fleck, J. Wansapura, P. Klimeczek, H. R. Al-Khalidi, E. S. Chung, et al.
Comparison of Magnetic Resonance Feature Tracking for Strain Calculation With Harmonic Phase Imaging Analysis
J. Am. Coll. Cardiol. Img.,
February 1, 2010;
3(2):
144 - 151.
[Abstract]
[Full Text]
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Abstract
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