Initial application of three-dimensional speckle-tracking echocardiography to detect subclinical left ventricular dysfunction and stratify cardiomyopathy associated with Duchenne muscular dystrophy in children
Three-dimensional (3D) speckle-tracking echocardiography (STE) is a new imaging modality used for quantitative analysis of left ventricular (LV) function. The aim of this study is to assess the value of 3D STE in early detection of subclinical myocardial involvement in children with Duchenne muscular dystrophy (DMD). Fifty-six children with DMD (mean age, 8.8 ± 1.9 years) and 31 age-matched control subjects were studied. Patients were subdivided into two groups by age: ≤ 8 or > 8 years. Standard echocardiography examinations were performed to measure LV size and ejection fraction (EF). 3D STE was performed to assess LV 3D global strain and LV end-diastolic volume (EDV), end-systolic volume (ESV), and EF. Standard and 3D echocardiography measures were compared between children with DMD and those in the control group as well as between different patient groups. The areas under the receiver-operating characteristic (ROC) curve were calculated to determine the capability of 3D global strain indices to discriminate between patients and control subjects. No significant difference was detected in either LVEF derived from M-mode or 3D echocardiography between the two groups, and they were both within the normal range. Compared with control subjects, children with DMD had significantly reduced LV 3D global longitudinal strain (GLS; − 16.6 ± 4.7 vs. − 19.5 ± 3.7, p = 0.003), global circumferential strain (GCS; − 13.7 ± 2.9 vs. − 15.8 ± 2.6, p = 0.001), global radial strain (GRS; 42.5 ± 9.7 vs. 50.3 ± 10.4, p = 0.001), and global area strain (GAS; − 25.3 ± 4.9 vs. − 30.7 ± 4.1, p = 0.000). The older DMD children (age > 8 years) had lower GLS (− 15.1 ± 4.43 vs. − 18.6 ± 4.35, p < 0.05), GCS (− 12.8 ± 3.48 vs. − 14.8 ± 2.83, p < 0.001), GAS (− 23.8 ± 4.7 vs. − 29.0 ± 5.4, p < 0.001), and GRS (40.7 ± 8.8 vs. 47.3 ± 11.5, p < 0.05) than younger patients (age ≤ 8 years). The AUC of GAS was 0.80, and the cutoff value of − 29.5 had a sensitivity of 85.7% and a specificity of 71.0% for differentiating DMD patients from control. 3D speckle-tracking echocardiography is useful for detecting subclinical myocardial dysfunction and stratifying cardiomyopathy in children with DMD.
Three-dimensional speckle-tracking echocardiography Cardiomyopathy Duchenne muscular dystrophy Area strain Children
This is a preview of subscription content, log in to check access.
This study was funded by Shenzhen Municipal Science and Technology Innovation Committee Foundation (No. JCYJ20140416141331487).
Compliance with ethical standards
Conflict of interest
The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
Cohen N, Muntoni F (2004) Multiple pathogenetic mechanisms in X linked dilated cardiomyopathy. Heart 90:835–841CrossRefGoogle Scholar
Muntoni F (2003) Cardiac complications of childhood myopathies. J Child Neurol 18:191–202CrossRefGoogle Scholar
Yiu EM, Kornberg AJ (2015) Duchenne muscular dystrophy. J Paediatr Child Health 51:759–764CrossRefGoogle Scholar
Eagle M, Baudouin SV, Chandler C, Giddings DR, Bullock R, Bushby K (2002) Survival in Duchenne muscular dystrophy: improvements in life expectancy since 1967 and the impact of home nocturnal ventilation. Neuromuscul Disord 12:926–929CrossRefGoogle Scholar
Spurney C, Shimizu R, Morgenroth LP, Kolski H, Gordish-Dressman H, Clemens PR (2014) Cooperative International Neuromuscular Research Group Duchenne natural history study demonstrates insufficient diagnosis and treatment of cardiomyopathy in Duchenne muscular dystrophy. Muscle Nerve 50:250–256CrossRefGoogle Scholar
Towbin JA (2003) A noninvasive means of detecting preclinical cardiomyopathy in Duchenne muscular dystrophy? J Am Coll Cardiol 42:317–318CrossRefGoogle Scholar
Jefferies JL, Eidem BW, Belmont JW, Craigen WJ, Ware SM, Fernbach SD et al (2005) Genetic predictors and remodeling of dilated cardiomyopathy in muscular dystrophy. Circulation 112:2799–2804CrossRefGoogle Scholar
Mori K, Hayabuchi Y, Inoue M, Suzuki M, Sakata M, Nakagawa R et al (2007) Myocardial strain imaging for early detection of cardiac involvement in patients with Duchenne’s progressive muscular dystrophy. Echocardiography 24:598–608CrossRefGoogle Scholar
Ryan TD, Taylor MD, Mazur W, Cripe LH, Pratt J, King EC et al (2013) Abnormal circumferential strain is present in young Duchenne muscular dystrophy patients. Ped Cardiol 34:1159–1165CrossRefGoogle Scholar
Hor KN, Wansapura J, Markham LW, Mazur W, Cripe LH, Fleck R et al (2009) Circumferential strain analysis identifies strata of cardiomyopathy in Duchenne muscular dystrophy: a cardiac magnetic resonance tagging study. J Am Coll Cardiol 53:1204–1210CrossRefGoogle Scholar
Schueler R, Sinning JM, Momcilovic D, Weber M, Ghanem A, Werner N et al (2012) Three-dimensional speckle-tracking analysis of left ventricular function after transcatheter aortic valve implantation. J Am Soc Echocardiogr 25(8):827–834CrossRefGoogle Scholar
Li SN, Wong SJ, Cheung YF (2011) Novel area strain based on three-dimensional wall motion analysis for assessment of global left ventricular performance after repair of tetralogy of Fallot. J Am Soc Echocardiogr 24:819–825CrossRefGoogle Scholar
Wen H, Liang Z, Zhao Y, Yang K (2011) Feasibility of detecting early left ventricular systolic dysfunction using global area strain: a novel index derived from three-dimensional speckle-tracking echocardiography. Eur J Echocardiogr 12:910–916CrossRefGoogle Scholar
Yamamoto T, Tanaka H, Matsumoto K, Lee T, Awano H, Yagi M et al (2013) Utility of transmural myocardial strain profile for prediction of early left ventricular dysfunction in patients with Duchenne muscular dystrophy. Am J Cardiol 111:902–907CrossRefGoogle Scholar
Silva MC, Meira ZM, Gurgel Giannetti J, da Silva MM, Campos AF, Barbosa Mde M et al (2007) Myocardial delayed enhancement by magnetic resonance imaging in patients with muscular dystrophy. J Am Coll Cardiol 49:1874–1879CrossRefGoogle Scholar
Fong PY, Turner PR, Denetclaw WF, Steinhardt R (1990) Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250:673–676CrossRefGoogle Scholar
Williams IA, Allen DG (2007) The role of reactive oxygen species in the hearts of dystrophin-deficient mdx mice. Am J Physiol Heart Circ Physiol 293:H1969–H1977CrossRefGoogle Scholar
Shigihara-Yasuda K, Tonoki H, Goto Y, Arahata K, Ishikawa N, Kajii N et al (1992) A symptomatic female patient with Duchenne muscular dystrophy diagnosed by dystrophin-staining: a case report. Eur J Pediatr 151:66–68CrossRefGoogle Scholar
Finsterer J, Stollberger C (2003) The heart in human dystrophinopathies. Cardiology 99:11–19CrossRefGoogle Scholar
Cheung YF (2012) The role of 3D wall motion tracking in heart failure. Nat Rev Cardiol 9:644–657CrossRefGoogle Scholar
Leitman M, Lysyansky P, Sidenko S, Shir V, Peleg E, Binenbaum M et al (2004) Two-dimensional strain—a novel software for real-time quantitative echocardiographic assessment of myocardial function. J Am Soc Echocardiogr 17:1021–1029CrossRefGoogle Scholar
Amundsen BH, Helle-Valle T, Edvardsen T, Torp H, Crosby J, Lyseggen E et al (2006) Noninvasive myocardial strain measurement by speckle tracking echocardiography: validation against sonomicrometry and tagged magnetic resonance imaging. J Am Coll Cardiol 47:789–793CrossRefGoogle Scholar
Yu HK, Yu W, Cheuk DK, Wong SJ, Chan GC, Cheung YF (2013) New three-dimensional speckle- tracking echocardiography identifies global impairment of left ventricular mechanics with a high sensitivity in childhood cancer survivors. J Am Soc Echocardiogr 26:846–852CrossRefGoogle Scholar
Yu W, Wong SJ, Cheung YF (2014) Left ventricular mechanics in adolescents and young adults with a history of kawasaki disease: analysis by three-dimensional speckle tracking echocardiography. Echocardiography 31:483–491CrossRefGoogle Scholar
Saha SK, Kiotsekoglou A, Toole RS, Moggridge JC, Nichols KJ, Govind S et al (2012) Value of two-dimensional speckle tracking and real time three-dimensional echocardiography for the identification of subclinical left ventricular dysfunction in patients referred for routine echocardiography. Echocardiography 29:588–597CrossRefGoogle Scholar
Christopher F, McCaffrey FM, Cnaan A, Morgenroth LP, Ghelani SJ, Gordish-Dressman H et al (2015) Feasibility and reproducibility of echocardiographic measures in children with muscular dystrophies. J Am Soc Echocardiogr 28:999–1008CrossRefGoogle Scholar
Gorcsan J-rd, Tanaka H (2011) Echocardiographic assessment of myocardial strain. J Am Coll Cardiol 58:1401–1413CrossRefGoogle Scholar
Huang BT, Yao HM, Huang H (2014) Left ventricular remodeling and dysfunction in systemic lupus erythematosus: a three-dimensional speckle tracking study. Echocardiography 31:1085–1094CrossRefGoogle Scholar
Dec GW (2013) Steroid therapy effectively delays Duchenne’s cardiomyopathy. J Am Coll Cardiol 61:955–956CrossRefGoogle Scholar
Duboc D, Meune C, Lerebours G, Devaux JY, Vaksmann G, Becane HM (2005) Effect of perindopril on the onset and progression of left ventricular dysfunction in Duchenne muscular dystrophy. J Am Coll Cardiol 45:855–857CrossRefGoogle Scholar
Duboc D, Meune C, Pierre B, Wahbi K, Eymard B, Toutain A et al (2007) Perindopril preventive treatment on mortality in Duchenne muscular dystrophy: 10 years’ follow-up. Am Heart J 154:596–602CrossRefGoogle Scholar
Janssen PM, Murray JD, Schill KE, Rastogi N, Schultz EJ, Tran T et al (2014) Prednisolone attenuates improvement of cardiac and skeletal contractile function and histopathology by lisinopril and spironolactone in the mdx mouse model of Duchenne muscular dystrophy. PLoS ONE 9(2):e88360CrossRefGoogle Scholar