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Diagnostic and Prognostic Value of Cardiovascular Magnetic Resonance in Neuromuscular Cardiomyopathies

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Abstract

Neuromuscular diseases (NMD) encompass a broad spectrum of diseases with variable type of cardiac involvement and there is lack of clinical data on Cardiovascular Magnetic Resonance (CMR) phenotypes or even prognostic value of CMR in NMD. We explored the diagnostic and prognostic value of CMR in NMD-related cardiomyopathies. The study included retrospective analysis of a cohort of 111 patients with various forms of NMD; mitochondrial: n = 14, Friedreich’s ataxia (FA): n = 27, myotonic dystrophy: n = 27, Becker/Duchenne’s muscular dystrophy (BMD/DMD): n = 15, Duchenne’s carriers: n = 6, other: n = 22. Biventricular volumes and function and myocardial late gadolinium enhancement (LGE) pattern and extent were assessed by CMR. Patients were followed-up for the composite clinical endpoint of death, heart failure development or need for permanent pacemaker/intracardiac defibrillator. The major NMD subtypes, i.e. FA, mitochondrial, BMD/DMD, and myotonic dystrophy had significant differences in the incidence of LGE (56%, 21%, 62% & 30% respectively, chi2 = 9.86, p = 0.042) and type of cardiomyopathy phenotype (chi2 = 13.8, p = 0.008), extent/pattern (p = 0.006) and progression rate of LGE (p = 0.006). In survival analysis the composite clinical endpoint differed significantly between NMD subtypes (p = 0.031), while the subgroup with LGE + and LVEF < 50% had the worst prognosis (Log-rank p = 0.0034). We present data from a unique cohort of NMD patients and provide evidence on the incidence, patterns, and the prognostic value of LGE in NMD-related cardiomyopathy. LGE is variably present in NMD subtypes and correlates with LV remodelling, dysfunction, and clinical outcomes in patients with NMD.

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All data are available upon reasonable request from the corresponding author.

References

  1. Feingold B, Mahle WT, Auerbach S, Clemens P, Domenighetti AA, Jefferies JL, Judge DP, Lal AK, Markham LW, Parks WJ, Tsuda T, Wang PJ, Yoo SJ, American Heart Association Pediatric Heart Failure Committee of the Council on Cardiovascular Disease in the Y, Council on Clinical C, Council on Cardiovascular R, Intervention, Council on Functional G, Translational B, Stroke C (2017) Management of Cardiac involvement associated with neuromuscular diseases: a scientific statement from the American Heart Association. Circulation 136(13):e200–e231

    Article  Google Scholar 

  2. Nikolaidou C, Karamitsos TD (2020) Cardiac magnetic resonance in patients with muscular dystrophies: strengthening the data. Eur J Prev Cardiol. https://doi.org/10.1177/2047487320932693

    Article  PubMed  Google Scholar 

  3. Grigoratos C, Aimo A, Barison A, Castiglione V, Todiere G, Ricci G, Siciliano G, Emdin M (2020) Cardiac magnetic resonance in patients with muscular dystrophies. Eur J Prev Cardiol. https://doi.org/10.1177/2047487320923052

    Article  Google Scholar 

  4. Cardona A, Arnold WD, Kissel JT, Raman SV, Zareba KM (2019) Myocardial fibrosis by late gadolinium enhancement cardiovascular magnetic resonance in myotonic muscular dystrophy type 1: highly prevalent but not associated with surface conduction abnormality. J Cardiovasc Magn Reson 21(1):26

    Article  Google Scholar 

  5. Luetkens JA, von Landenberg C, Isaak A, Faron A, Kuetting D, Gliem C, Dabir D, Kornblum C, Thomas D (2019) Comprehensive cardiac magnetic resonance for assessment of cardiac involvement in myotonic muscular dystrophy type 1 and 2 without known cardiovascular disease. Circ Cardiovasc Imaging. https://doi.org/10.1161/CIRCIMAGING.119.009100

    Article  PubMed  Google Scholar 

  6. Verhaert D, Richards K, Rafael-Fortney JA, Raman SV (2011) Cardiac involvement in patients with muscular dystrophies: magnetic resonance imaging phenotype and genotypic considerations. Circ Cardiovasc Imaging 4(1):67–76

    Article  Google Scholar 

  7. Yilmaz A, Gdynia H-J, Ludolph AC, Klingel K, Kandolf R, Sechtem U (2010) Cardiomyopathy in a Duchenne muscular dystrophy carrier and her diseased son: similar pattern revealed by cardiovascular MRI. Circulation. https://doi.org/10.1161/CIR.0b013e3181d74468

    Article  PubMed  Google Scholar 

  8. Aikawa T, Takeda A, Oyama-Manabe N, Naya M, Yamazawa H, Koyanagawa K, Ito YM, Anzai T (2019) Progressive left ventricular dysfunction and myocardial fibrosis in Duchenne and Becker muscular dystrophy: a longitudinal cardiovascular magnetic resonance study. Pediatr Cardiol 40(2):384–392

    Article  Google Scholar 

  9. Casazza F, Morpurgo M (1996) The varying evolution of friedreich’s ataxia cardiomyopathy. Am J Cardiol 77(10):895–898

    Article  CAS  Google Scholar 

  10. Child JS, Perloff JK, Bach PM, Wolfe AD, Perlman S, Pieter Kark RA (1986) Cardiac involvement in Friedreich’s ataxia: A clinical study of 75 patients. J Am Coll Cardiol 7(6):1370–1378

    Article  CAS  Google Scholar 

  11. Kramer CM, Barkhausen J, Bucciarelli-Ducci C, Flamm SD, Kim RJ, Nagel E (2020) Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reson 22(1):17

    Article  Google Scholar 

  12. Maceira AM, Prasad SK, Khan M, Pennell DJ (2006) Normalized left ventricular systolic and diastolic function by steady state free precession cardiovascular magnetic resonance. J Cardiovasc Magn Reson 8(3):417–426

    Article  CAS  Google Scholar 

  13. Antonopoulos AS, Azzu A, Androulakis E, Tanking C, Papagkikas P, Mohiaddin RH (2021) Eosinophilic heart disease: diagnostic and prognostic assessment by cardiac magnetic resonance. Eur Heart J Cardiovasc Imaging. https://doi.org/10.1093/ehjci/jeaa346

    Article  PubMed  Google Scholar 

  14. Grani C, Eichhorn C, Biere L, Kaneko K, Murthy VL, Agarwal V, Aghayev A, Steigner M, Blankstein R, Jerosch-Herold M, Kwong RY (2019) Comparison of myocardial fibrosis quantification methods by cardiovascular magnetic resonance imaging for risk stratification of patients with suspected myocarditis. J Cardiovasc Magn Reson 21(1):14

    Article  Google Scholar 

  15. Core-Team R. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. URL https://www.R-project.org/. Accessed 31 Jul 2021

  16. Giglio V, Puddu PE, Camastra G, Sbarbati S, Della Sala SW, Ferlini A, Gualandi F, Ricci E, Sciarra F, Ansalone G, Di Gennaro M (2014) Patterns of late gadolinium enhancement in Duchenne muscular dystrophy carriers. J Cardiovasc Magn Reson 16(1):45

    Article  Google Scholar 

  17. Choudhary P, Nandakumar R, Greig H, Broadhurst P, Dean J, Puranik R, Celermajer DS, Hillis GS (2016) Structural and electrical cardiac abnormalities are prevalent in asymptomatic adults with myotonic dystrophy. Heart 102(18):1472–1478

    Article  CAS  Google Scholar 

  18. Cohen BH, Gold DR (2001) Mitochondrial cytopathy in adults: what we know so far. Clevel Clin J Med 68(7):625–626

    Article  CAS  Google Scholar 

  19. Blaszczyk E, Grieben U, von Knobelsdorff-Brenkenhoff F, Kellman P, Schmacht L, Funk S, Spuler S, Schulz-Menger J (2019) Subclinical myocardial injury in patients with Facioscapulohumeral muscular dystrophy 1 and preserved ejection fraction—assessment by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 21(1):25

    Article  Google Scholar 

  20. Florian A, Ludwig A, Engelen M, Waltenberger J, Rösch S, Sechtem U, Yilmaz A (2014) Left ventricular systolic function and the pattern of late-gadolinium-enhancement independently and additively predict adverse cardiac events in muscular dystrophy patients. J Cardiovasc Magn Reson 16(1):81

    Article  Google Scholar 

  21. Florian AR, Ludwig A, Rösch S, Sechtem U, Yilmaz A (2015) Differences in cardiac involvement between carriers of Duchenne and Becker muscular dystrophy - a cardiovascular magnetic resonance study. J Cardiovasc Magn Reson 17(S1):Q90

    Article  Google Scholar 

  22. Marty B, Gilles R, Toussaint M, Béhin A, Stojkovic T, Eymard B, Carlier PG, Wahbi K (2019) Comprehensive evaluation of structural and functional myocardial impairments in Becker muscular dystrophy using quantitative cardiac magnetic resonance imaging. Eur Heart J Cardiovasc Imaging 20(8):906–915

    Article  Google Scholar 

  23. Petri H, Ahtarovski KA, Vejlstrup N, Vissing J, Witting N, Køber L, Bundgaard H (2014) Myocardial fibrosis in patients with myotonic dystrophy type 1: a cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. https://doi.org/10.1186/s12968-014-0059-z

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rosales XQ, Moser SJ, Tran T, McCarthy B, Dunn N, Habib P, Simonetti OP, Mendell JR, Raman SV (2011) Cardiovascular magnetic resonance of cardiomyopathy in limb girdle muscular dystrophy 2B and 2I. J Cardiovasc Magn Reson 13(1):39

    Article  Google Scholar 

  25. Weidemann F, Rummey C, Bijnens B, Störk S, Jasaityte R, Dhooge J, Baltabaeva A, Sutherland G, Schulz JB, Meier T (2012) The heart in Friedreich ataxia: definition of cardiomyopathy, disease severity, and correlation with neurological symptoms. Circulation 125(13):1626–1634

    Article  Google Scholar 

  26. Mordi I, Bezerra H, Carrick D, Tzemos N (2015) The combined incremental prognostic value of LVEF, late gadolinium enhancement, and global circumferential strain assessed by CMR. JACC Cardiovasc Imaging 8(5):540–549

    Article  Google Scholar 

  27. Romano S, Judd RM, Kim RJ, Kim HW, Klem I, Heitner JF, Shah DJ, Jue J, White BE, Indorkar R, Shenoy C, Farzaneh-Far A (2018) Feature-tracking global longitudinal strain predicts death in a multicenter population of patients with ischemic and nonischemic dilated cardiomyopathy incremental to ejection fraction and late gadolinium enhancement. JACC Cardiovasc Imaging 11(10):1419–1429

    Article  Google Scholar 

  28. Shanbhag SM, Greve AM, Aspelund T, Schelbert EB, Cao JJ, Danielsen R, Thornorgeirsson G, Sigurethsson S, Eiriksdottir G, Harris TB, Launer LJ, Guethnason V, Arai AE (2019) Prevalence and prognosis of ischaemic and non-ischaemic myocardial fibrosis in older adults. Eur Heart J 40(6):529–538

    Article  CAS  Google Scholar 

  29. de Waha S, Desch S, Eitel I, Fuernau G, Zachrau J, Leuschner A, Gutberlet M, Schuler G, Thiele H (2010) Impact of early vs. late microvascular obstruction assessed by magnetic resonance imaging on long-term outcome after ST-elevation myocardial infarction: a comparison with traditional prognostic markers. Eur Heart J 31(21):2660–8

    Article  Google Scholar 

  30. Becker MAJ, Cornel JH, van de Ven PM, van Rossum AC, Allaart CP, Germans T (2018) The prognostic value of late gadolinium-enhanced cardiac magnetic resonance imaging in nonischemic dilated cardiomyopathy: a review and meta-analysis. JACC Cardiovasc Imaging 11(9):1274–1284

    Article  Google Scholar 

  31. Aquaro GD, Perfetti M, Camastra G, Monti L, Dellegrottaglie S, Moro C, Pepe A, Todiere G, Lanzillo C, Scatteia A, Di Roma M, Pontone G, Perazzolo Marra M, Barison A, Di Bella G, Cardiac Magnetic Resonance Working Group of the Italian Society of C (2017) Cardiac MR with late gadolinium enhancement in acute myocarditis with preserved systolic function: ITAMY study. J Am Coll Cardiol 70(16):1977–1987

    Article  Google Scholar 

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Author notes

  1. Batool Almogheer and Alexios S. Antonopoulos have equally contributed to this work.

Authors and Affiliations

  1. CMR Unit, Royal Brompton and Harefield Hospital NHS Foundation Trust, Sydney Street, Chelsea, London, SW3 6NP, UK

    Batool Almogheer, Alexios S. Antonopoulos, Alessia Azzu, Safaa Al Mohdar & Raad H. Mohiaddin

  2. National Heart and Lung Institute, Imperial College London, London, UK

    Alessia Azzu & Raad H. Mohiaddin

  3. Unit of Inherited Cardiac Conditions, 1st Cardiology Department, University of Athens, Athens, Greece

    Alexios S. Antonopoulos & Charalambos Vlachopoulos

  4. Cardiomyopathy Unit, Cardiology Department, Royal Brompton Hospital, London, UK

    Antonios Pantazis

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  1. Batool Almogheer
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Contributions

BA collected the data and performed the image analysis, ASA performed statistical analysis and wrote the manuscript, AA contributed to image analysis, SAM contributed to data collection; CV & AP critically reviewed and edited the manuscript. RHM conceived the idea, supervised the project and critically reviewed and edited the manuscript.

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Correspondence to Raad H. Mohiaddin.

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The authors declare that they have no conflict of interest.

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The study was registered as a Clinical Audit by the Quality and Safety. Department of the Royal Brompton Hospital.

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Almogheer, B., Antonopoulos, A.S., Azzu, A. et al. Diagnostic and Prognostic Value of Cardiovascular Magnetic Resonance in Neuromuscular Cardiomyopathies. Pediatr Cardiol 43, 27–38 (2022). https://doi.org/10.1007/s00246-021-02686-y

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