Skip to main content
SpringerLink
Log in

Assessment of left ventricular dyssynchrony by speckle tracking echocardiography in children with duchenne muscular dystrophy

  • Original Paper
  • Published:
The International Journal of Cardiovascular Imaging Aims and scope Submit manuscript

Abstract

Prognosis of Duchenne muscular dystrophy (DMD) is related to cardiac dysfunction. Two dimensional-speckle tracking echocardiography (2D-STE) has recently emerged as a non-invasive functional biomarker for early detection of DMD-related cardiomyopathy. This study aimed to determine, in DMD children, the existence of left ventricle (LV) dyssynchrony using 2D-STE analysis. This prospective controlled study enrolled 25 boys with DMD (mean age 11.0 ± 3.5 years) with normal LV ejection fraction and 50 age-matched controls. Three measures were performed to assess LV mechanical dyssynchrony: the opposing-wall delays (longitudinal and radial analyses), the modified Yu index, and the time-to-peak delays of each segment. Feasibility and reproducibility of 2D-STE dyssynchrony were evaluated. All three mechanical dyssynchrony criteria were significantly higher in the DMD group than in healthy subjects: (1) opposing-wall delays in basal inferoseptal to basal anterolateral segments (61.4 ± 45.3 ms vs. 18.3 ± 50.4 ms, P < 0.001, respectively) and in mid inferoseptal to mid anterolateral segments (58.6 ± 35.3 ms vs. 42.4 ± 36.4 ms, P < 0.05, respectively), (2) modified Yu index (33.3 ± 10.1 ms vs. 28.5 ± 8.1 ms, P < 0.05, respectively), and (3) most of time-to-peak values, especially in basal and mid anterolateral segments. Feasibility was excellent and reliability was moderate to excellent, with ICC values ranging from 0.49 to 0.97. Detection of LV mechanical dyssynchrony using 2D-STE analysis is an easily and reproducible method in paediatric DMD. The existence of an early LV mechanical dyssynchrony visualized using 2D-STE analysis in children with DMD before the onset of cardiomyopathy represents a perspective for future paediatric drug trials in the DMD-related cardiomyopathy prevention.

Clinical Trial Registration Clinicaltrials.gov NCT02418338. Post-hoc study, registered on April 16, 2015.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig.2

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Abbreviations

2D-strain:

Two-dimensional strain

2D-STE:

Two-dimensional speckle tracking echocardiography

ACE:

Angiotensin converting enzyme.

CRT:

Cardiac resynchronization therapy

DMD:

Duchenne muscular dystrophy

ECG:

Electrocardiogram

ICC:

Intraclass correlation coefficient

LV:

Left ventricle

LVEF:

Left ventricle ejection fraction (biplane Simpson)

LVIDd:

Left ventricle internal diastolic diameter

RV:

Right ventricle

TDI:

Tissue Doppler imaging

VCFc:

Contraction velocity corrected by cardiac frequency

References

  1. Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, van Ommen G-JB, Kunkel LM (2015) The pathogenesis and therapy of muscular dystrophies. Annu Rev Genomics Hum Genet. 16:281–308

    Article  CAS  PubMed  Google Scholar 

  2. Kamdar F, Garry DJ (2016) Dystrophin-deficient cardiomyopathy. J Am Coll Cardiol 67:2533–2546

    Article  CAS  PubMed  Google Scholar 

  3. Spurney CF, 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 Off Publ Am Soc Echocardiogr 28:999–1008

    Article  Google Scholar 

  4. Connuck DM, Sleeper LA, Colan SD, Cox GF, Towbin JA, Lowe AM et al (2008) Characteristics and outcomes of cardiomyopathy in children with duchenne or becker muscular dystrophy: a comparative study from the pediatric cardiomyopathy registry. Am Heart J 155:998–1005

    Article  PubMed  PubMed Central  Google Scholar 

  5. Duboc D, Meune C, Lerebours G, Devaux J-Y, Vaksmann G, Bécane H-M (2005) Effect of perindopril on the onset and progression of left ventricular dysfunction in Duchenne muscular dystrophy. J Am Coll Cardiol 45:855–857

    Article  CAS  PubMed  Google Scholar 

  6. Amedro P, Vincenti M, De La Villeon G, Lavastre K, Barrea C, Guillaumont S et al (2019) Speckle-tracking echocardiography in children with duchenne muscular dystrophy: a prospective multicenter controlled cross-sectional study. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 32:412–422

    Article  Google Scholar 

  7. Mertens L, Ganame J, Claus P, Goemans N, Thijs D, Eyskens B et al (2008) Early regional myocardial dysfunction in young patients with Duchenne muscular dystrophy. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 21:1049–1054

    Article  Google Scholar 

  8. Chang S-A, Kim H-K, Kim D-H, Kim Y-J, Sohn D-W, Oh B-H et al (2009) Left ventricular systolic and diastolic dyssynchrony in asymptomatic hypertensive patients. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 22:337–342

    Article  Google Scholar 

  9. Wang J, Kurrelmeyer KM, Torre-Amione G, Nagueh SF (2007) Systolic and diastolic dyssynchrony in patients with diastolic heart failure and the effect of medical therapy. J Am Coll Cardiol 49:88–96

    Article  PubMed  Google Scholar 

  10. Edvardsen T, Helle-Valle T, Smiseth OA (2006) Systolic dysfunction in heart failure with normal ejection fraction: speckle-tracking echocardiography. Prog Cardiovasc Dis 49:207–214

    Article  PubMed  Google Scholar 

  11. Yu CM, Bax JJ, Monaghan M, Nihoyannopoulos P (2004) Echocardiographic evaluation of cardiac dyssynchrony for predicting a favourable response to cardiac resynchronisation therapy. Heart. 90:vi17-22

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vardas PE, Auricchio A, Blanc J-J, Daubert J-C, Drexler H, Ector H et al (2007) Guidelines for cardiac pacing and cardiac resynchronization therapy: the task force for cardiac pacing and cardiac resynchronization therapy of the european society of cardiology. Developed in collaboration with the european heart rhythm association. Eur Heart J. 28:2256–2295

    Article  PubMed  Google Scholar 

  13. Littmann L, Symanski JD (2000) Hemodynamic implications of left bundle branch block. J Electrocardiol 33:115–121

    Article  PubMed  Google Scholar 

  14. Saxon LA, Kerwin WF, Cahalan MK, Kalman JM, Olgin JE, Foster E et al (1998) Acute effects of intraoperative multisite ventricular pacing on left ventricular function and activation/contraction sequence in patients with depressed ventricular function. J Cardiovasc Electrophysiol 9:13–21

    Article  CAS  PubMed  Google Scholar 

  15. Kerwin WF, Botvinick EH, O’Connell JW, Merrick SH, DeMarco T, Chatterjee K et al (2000) Ventricular contraction abnormalities in dilated cardiomyopathy: effect of biventricular pacing to correct interventricular dyssynchrony. J Am Coll Cardiol 35:1221–1227

    Article  CAS  PubMed  Google Scholar 

  16. 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 154:596–602

    Article  CAS  PubMed  Google Scholar 

  17. Birnkrant DJ, Bushby K, Bann CM, Apkon SD, Blackwell A, Brumbaugh D et al (2018) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and neuromuscular, rehabilitation, endocrine, and gastrointestinal and nutritional management. Lancet Neurol 17:251–267

    Article  PubMed  PubMed Central  Google Scholar 

  18. Lopez L, Colan SD, Frommelt PC, Ensing GJ, Kendall K, Younoszai AK et al (2010) Recommendations for quantification methods during the performance of a pediatric echocardiogram: a report from the pediatric measurements writing group of the american society of echocardiography pediatric and congenital heart disease council. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr. 23:465–95

    Article  Google Scholar 

  19. Voigt J-U, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R et al (2015) Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/industry task force to standardize deformation imaging. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 28:183–193

    Article  Google Scholar 

  20. Chubb H, Ceresnak SR, Motonaga KS, Dubin AM (2020) A proposed method for the calculation of age-dependent QRS duration z-scores. J Electrocardiol 58:132–134

    Article  PubMed  Google Scholar 

  21. Borys S, Rory C, Deal BJ, Gettes LS (2009) AHA/ACCF/HRS recommendations for the standardization and interpretation of the electrocardiogram. Circulation Am Heart Assoc 119:235–40

    Google Scholar 

  22. Thomas TO, Jefferies JL, Lorts A, Anderson JB, Gao Z, Benson DW et al (2015) Autonomic dysfunction: a driving force for myocardial fibrosis in young duchenne muscular dystrophy patients? Pediatr Cardiol 36:561–568

    Article  PubMed  Google Scholar 

  23. Thomas VC, Cumbermack KM, Lamphier CK, Phillips CR, Fyfe DA, Fornwalt BK (2013) Measures of dyssynchrony in the left ventricle of healthy children and young patients with dilated cardiomyopathy. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 26:142–153

    Article  Google Scholar 

  24. Tanaka H, Nesser H-J, Buck T, Oyenuga O, Jánosi RA, Winter S et al (2010) Dyssynchrony by speckle-tracking echocardiography and response to cardiac resynchronization therapy: results of the Speckle Tracking and Resynchronization (STAR) study. Eur Heart J 31:1690–1700

    Article  PubMed  PubMed Central  Google Scholar 

  25. Risum N, Jons C, Olsen NT, Fritz-Hansen T, Bruun NE, Hojgaard MV et al (2012) Simple regional strain pattern analysis to predict response to cardiac resynchronization therapy: rationale, initial results, and advantages. Am Heart J 163:697–704

    Article  PubMed  Google Scholar 

  26. Yu C-M, Chau E, Sanderson JE, Fan K, Tang M-O, Fung W-H et al (2002) Tissue Doppler echocardiographic evidence of reverse remodeling and improved synchronicity by simultaneously delaying regional contraction after biventricular pacing therapy in heart failure. Circulation 105:438–445

    Article  PubMed  Google Scholar 

  27. Bharucha T, Khan R, Mertens L, Friedberg MK (2013) Right Ventricular Mechanical Dyssynchrony and Asymmetric Contraction in Hypoplastic Heart Syndrome are Associated with Tricuspid Regurgitation. J Am Soc Echocardiogr 26:1214–1220

    Article  PubMed  Google Scholar 

  28. Zhang X, Ha S, Wang X, Shi Y, Duan S, Li Z (2015) Speckle tracking echocardiography: clinical applications in cardiac resynchronization therapy. Int J Clin Exp Med 8:6668–6676

    PubMed  PubMed Central  Google Scholar 

  29. Suffoletto MS, Dohi K, Cannesson M, Saba S, Gorcsan J (2006) Novel speckle-tracking radial strain from routine black-and-white echocardiographic images to quantify dyssynchrony and predict response to cardiac resynchronization therapy. Circulation 113:960–968

    Article  PubMed  Google Scholar 

  30. Gorcsan J, Oyenuga O, Habib PJ, Tanaka H, Adelstein EC, Hara H et al (2010) The relationship of echocardiographic dyssynchrony to long-term survival following cardiac resynchronization therapy. Circulation 122:1910–1918

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gorcsan J, Tanabe M, Bleeker GB, Suffoletto MS, Thomas NC, Saba S et al (2007) Combined longitudinal and radial dyssynchrony predicts ventricular response after resynchronization therapy. J Am Coll Cardiol 50:1476–1483

    Article  PubMed  Google Scholar 

  32. Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428

    Article  CAS  PubMed  Google Scholar 

  33. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163

    Article  PubMed  PubMed Central  Google Scholar 

  34. Hor KN, Wansapura JP, Al-Khalidi HR, Gottliebson WM, Taylor MD, Czosek RJ et al (2011) Presence of mechanical dyssynchrony in Duchenne muscular dystrophy. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson 13:12

    Google Scholar 

  35. Bilchick KC, Salerno M, Plitt D, Dori Y, Crawford TO, Drachman D et al (2011) Prevalence and distribution of regional scar in dysfunctional myocardial segments in Duchenne muscular dystrophy. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson 13:20

    Google Scholar 

  36. Frankel KA, Rosser RJ (1976) The pathology of the heart in progressive muscular dystrophy: epimyocardial fibrosis. Hum Pathol 7:375–386

    Article  CAS  PubMed  Google Scholar 

  37. Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, Metzger JM (2005) Dystrophic heart failure blocked by membrane sealant poloxamer. Nature 436:1025–1029

    Article  CAS  PubMed  Google Scholar 

  38. Bilchick KC, Saha SK, Mikolajczyk E, Cope L, Ferguson WJ, Yu W et al (2006) Differential regional gene expression from cardiac dyssynchrony induced by chronic right ventricular free wall pacing in the mouse. Physiol Genom 26:109–115

    Article  CAS  Google Scholar 

  39. Wilke L, Abellan Schneyder FE, Roskopf M, Jenke AC, Heusch A, Hensel KO (2018) Speckle tracking stress echocardiography in children: interobserver and intraobserver reproducibility and the impact of echocardiographic image quality. Sci Rep 8:1–12

    Article  CAS  Google Scholar 

  40. Bleeker GB, Yu C-M, Nihoyannopoulos P, de Sutter J, Van de Veire N, Holman ER et al (2007) Optimal use of echocardiography in cardiac resynchronisation therapy. Heart Br Card Soc 93:1339–1350

    Article  Google Scholar 

  41. Anderson LJ, Miyazaki C, Sutherland GR, Oh JK (2008) Patient selection and echocardiographic assessment of dyssynchrony in cardiac resynchronization therapy. Circulation 117:2009–2023

    Article  PubMed  Google Scholar 

  42. Stig U, Thor E, Hans T, Bjørn A, Smiseth Otto A (2000) Myocardial strain by doppler echocardiography. Circulation 102:1158–1164

    Article  Google Scholar 

  43. Edvardsen T, Skulstad H, Aakhus S, Urheim S, Ihlen H (2001) Regional myocardial systolic function during acute myocardial ischemia assessed by strain Doppler echocardiography. J Am Coll Cardiol 37:726–730

    Article  CAS  PubMed  Google Scholar 

  44. McNally EM, Kaltman JR, Benson DW, Canter CE, Cripe LH, Duan D et al (2015) Contemporary cardiac issues in Duchenne muscular dystrophy. Working group of the national heart, lung, and blood institute in collaboration with parent project muscular dystrophy. Circulation. 131:1590–1598

    Article  PubMed  PubMed Central  Google Scholar 

  45. Spurney C, Shimizu R, Morgenroth LP, Kolski H, Gordish-Dressman H, Clemens PR et al (2014) Cooperative International Neuromuscular Research Group Duchenne Natural History Study demonstrates insufficient diagnosis and treatment of cardiomyopathy in Duchenne muscular dystrophy. Muscle Nerve 50:250–256

    Article  PubMed  PubMed Central  Google Scholar 

  46. Viollet L, Thrush PT, Flanigan KM, Mendell JR, Allen HD (2012) Effects of angiotensin-converting enzyme inhibitors and/or beta blockers on the cardiomyopathy in Duchenne muscular dystrophy. Am J Cardiol 110:98–102

    Article  CAS  PubMed  Google Scholar 

  47. Ogata H, Ishikawa Y, Ishikawa Y, Minami R (2009) Beneficial effects of beta-blockers and angiotensin-converting enzyme inhibitors in Duchenne muscular dystrophy. J Cardiol 53:72–78

    Article  PubMed  Google Scholar 

  48. Matthews E, Brassington R, Kuntzer T, Jichi F, Manzur AY (2016) Corticosteroids for the treatment of Duchenne muscular dystrophy. Cochrane Database Syst Rev. CD003725

  49. Bleeker GB, Holman ER, Steendijk P, Boersma E, van der Wall EE, Schalij MJ et al (2006) Cardiac resynchronization therapy in patients with a narrow QRS complex. J Am Coll Cardiol 48:2243–2250

    Article  PubMed  Google Scholar 

  50. Yu C-M, Chan Y-S, Zhang Q, Yip GWK, Chan C-K, Kum LCC et al (2006) Benefits of cardiac resynchronization therapy for heart failure patients with narrow QRS complexes and coexisting systolic asynchrony by echocardiography. J Am Coll Cardiol 48:2251–2257

    Article  PubMed  Google Scholar 

  51. Bleeker GB, Kaandorp Theodorus AM, Lamb Hildo J, Eric B, Paul S, de Roos A et al (2006) Effect of posterolateral scar tissue on clinical and echocardiographic improvement after cardiac resynchronization therapy. Circulation Am Heart Assoc 113:969–976

    Google Scholar 

Download references

Acknowledgements

We thank all our patients and their families for their participation in the study, and Anne Cadene for the quality of study monitoring.

Funding

This work was supported by grants from Montpellier University Hospital Clinical Research Institutional Grant [PHRC-MERRI UF 9458] and from the French National Muscular Dystrophy Association [AFM 20225].

Author information

Author notes

  1. Alain Lacampagne and Pascal Amedro have contributed equally to the study.

Authors and Affiliations

  1. Paediatric and Adult Cardiology Department, M3C Regional Reference CHD Center, CHU Montpellier, Montpellier, France

    Nicolas Lanot, Marie Vincenti, Hamouda Abassi, Charlene Bredy, Audrey Agullo, Kathleen Lavastre & Gregoire De La Villeon

  2. PhyMedExp, University of Montpellier, CNRS, INSERM, CHU Montpellier, Montpellier, France

    Marie Vincenti, Hamouda Abassi, Pierre Meyer, François Rivier, Albano C. Meli, Jeremy Fauconnier, Olivier Cazorla & Alain Lacampagne

  3. Epidemiology and Clinical Research Department, CHU Montpellier, Montpellier, France

    Lucie Gamon

  4. Paediatric Cardiology and Rehabilitation Unit, Saint-Pierre Institute, Palavas-Les-Flots, France

    Gregoire De La Villeon

  5. Epidemiology and Clinical Research Department, CHU Nimes, Nimes, France

    Thibault Mura

  6. Paediatric and Congenital Cardiology Department, Cliniques Universitaires Saint-Luc, UCL University, Brussels, Belgium

    Catherine Barrea

  7. Paediatric Neurology, National Reference Center for Neuromuscular Diseases, CHU Montpellier, Montpellier, France

    Pierre Meyer & François Rivier

  8. Department of Paediatric and Adult Congenital Cardiology, M3C National Reference Centre, Bordeaux University Hospital, Haut Lévêque Hospital, Avenue de Magellan, 33604, Pessac Cedex, France

    Pascal Amedro

  9. University of Bordeaux, INSERM, Bordeaux Cardio-Thoracic Research Centre, U1045, Pessac, France

    Pascal Amedro

  10. IHU Liryc, Electrophysiology and Heart Modelling Institute, Fondation Bordeaux Université, Pessac, France

    Pascal Amedro

Authors
  1. Nicolas Lanot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie Vincenti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hamouda Abassi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charlene Bredy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Audrey Agullo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lucie Gamon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thibault Mura
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kathleen Lavastre
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gregoire De La Villeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Catherine Barrea
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Pierre Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. François Rivier
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Albano C. Meli
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jeremy Fauconnier
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Olivier Cazorla
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Alain Lacampagne
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Pascal Amedro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PA and AL conceived and designed the study. PA, JF, OC and AL obtained funding. PA supervised this work. NL and MV performed image acquisition and analysis. LG and TM performed the statistical analysis. PA, NL, MV, HA, GDLV, KL, ACM, OC, JF, and AL drafted the manuscript. All authors discussed the results and contributed to the final revision of the manuscript.

Corresponding author

Correspondence to Pascal Amedro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Consent to participate

Informed consent was obtained from all parents or legal guardians.

Consent for publication

Informed consent was obtained from all parents or legal guardians. Only anonymized data has been published.

Ethical approval

The study was conducted in compliance with the Good Clinical Practices protocol and Declaration of Helsinki principles. The South Mediterranean IV Ethics Committee (2014-A01764-44) in France and the UCL Ethics Committee (2016-28AVR-192) in Belgium approved the study, which was registered on ClinicalTrials.gov (NCT02418338)

Informed consent

Informed consent was obtained from all parents or legal guardians.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 90 KB)

Supplementary file2 (DOC 41 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lanot, N., Vincenti, M., Abassi, H. et al. Assessment of left ventricular dyssynchrony by speckle tracking echocardiography in children with duchenne muscular dystrophy. Int J Cardiovasc Imaging 38, 79–89 (2022). https://doi.org/10.1007/s10554-021-02369-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10554-021-02369-y

Keywords

Search

Navigation