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Novel Cardiac Magnetic Resonance Feature Tracking (CMR-FT) Analysis for Detection of Myocardial Fibrosis in Pediatric Hypertrophic Cardiomyopathy

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Abstract

Myocardial fibrosis is a risk factor for sudden cardiac death in hypertrophic cardiomyopathy (HCM) and is conventionally identified by cardiac magnetic resonance imaging (CMR) using late gadolinium enhancement (LGE). This study evaluates utility of a novel 16-segment CMR feature tracking (CMR-FT) technique for measuring left ventricular (LV) strain (S) and strain rate (SR) on non-contrast cine images to detect myocardial fibrosis in pediatric HCM. We hypothesized that CMR-FT-derived S and SR will accurately differentiate HCM patients with and without myocardial fibrosis. Consecutive children with HCM who underwent CMR with LGE at our institution from 2006 to 2014 were included. Global and regional longitudinal, radial and circumferential S and SR of the LV in 2D and 3D were obtained using a CMR-FT software. Comparisons were made between HCM patients with (+LGE) and without (−LGE) delayed enhancement. Of the 29 HCM patients (mean age 13.5 ± 6.1 years; 52 % males), 11 (40 %) patients (mean age 17.5 ± 8.4 years) had +LGE. Global longitudinal, circumferential and radial S and SR were lower in +LGE compared to −LGE patients, in both 2D and 3D. Regional analysis revealed lower segmental S and SR in the septum with fibrosis compared to free wall without fibrosis. A global longitudinal S of ≤ −12.8 had 91 % sensitivity and 89 % specificity for detection of LGE. In pediatric HCM patients with myocardial fibrosis, global LV longitudinal, circumferential and radial S and SR were reduced, specifically in areas of fibrosis. A global longitudinal S of ≤ −12.8 detected patients with fibrosis with high degree of accuracy. This novel CMR-FT technique may be useful to identify myocardial fibrosis and risk-stratify pediatric HCM without use of contrast agents.

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Abbreviations

CMR:

Cardiac magnetic resonance

FT:

Feature tracking

HCM:

Hypertrophic cardiomyopathy

LGE:

Late gadolinium enhancement

LV:

Left ventricle

SCD:

Sudden cardiac death

SSFP:

Steady-state free precession

S:

Peak systolic strain

SR:

Peak systolic strain rate

TDI:

Tissue Doppler imaging

References

  1. Almaas VM, Haugaa KH, Strom EH, Scott H, Smith HJ, Dahl CP, Geiran OR, Endresen K, Aakhus S, Amlie JP, Edvardsen T (2014) Noninvasive assessment of myocardial fibrosis in patients with obstructive hypertrophic cardiomyopathy. Heart 100:631–638

    Article  PubMed  Google Scholar 

  2. Almaas VM, Hauhaa KH, Strom EH, Scott H, Smith HJ, Dahl CP, Geiran OR, Endresen K, Aakhus S, Amlie JP, Edvardsen T (2014) Noninvasive assessment of myocardial fibrosis in patients with obstructive hypertrophic cardiomyopathy. Heart 100(8):631–638

    Article  PubMed  Google Scholar 

  3. Augustine D, Lewandowski AJ, Lazdam M, Rai A, Francis J, Myerson S, Noble A, Becher H, Neubauer S, Petersen SE, Leeson P (2013) Global and regional left ventricular myocardial deformation measures by magnetic resonance feature tracking in healthy volunteers: comparison with tagging and relevance of gender. J Cardiovasc Magn Reson 15:18

    Article  Google Scholar 

  4. Basso C, Thiene G, Corrado D, Buja G, Melacini P, Nava A (2000) Hypertrophic cardiomyopathy and sudden death in the young: pathologic evidence of myocardial ischemia. Hum Pathol 31:988–998

    Article  CAS  PubMed  Google Scholar 

  5. Bruder O, Wagner A, Jensen CJ, Schneider S, Ong P, Kispert EM, Nassenstein K, Schlosser T, Sabin GV, Sechtem U, Mahrholdt H (2010) Myocardial scar visualized by cardiovascular magnetic resonance imaging predicts major adverse events in patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 56:875–887

    Article  PubMed  Google Scholar 

  6. Buss SJ, Breuninger K, Lehrke S, Voss A, Galuschky C, Lossnitzer D, Andre F, Ehlermann P, Franke J, Taeger T, Frankenstein L, Steen H, Meder B, Giannitsis E, Katus HA, Korosoglou G (2014) Assessment of myocardial deformation with cardiac magnetic resonance strain imaging improves risk stratification in patients with dilated cardiomyopathy. Eur Heart J Cardiovasc Imaging 16:307–315

    Article  PubMed  Google Scholar 

  7. Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS (2002) Standardized Myocardial Segmentation and Nomenclature for Tomographic Imaging of the Heart. A statement for healthcare professionals from the cardiac imaging committee of the council on clinical cardiology of the American Heart Association. Circulation 105:539–542

    Article  PubMed  Google Scholar 

  8. Chan RH, Maron BJ, Olivotto I, Pencina MJ, Assenza GE, Haas T, Lesser JR, Gruner C, Crean AM, Rakowski H, Udelson JE, Rowin E, Lombardi M, Cecchi F, Tomberli B, Spirito P, Formisano F, Biagini E, Rapezzi C, De Cecco CN, Autore C, Cook EF, Hong SN, Gibson CM, Manning WJ, Appelbaum E, Maron MS (2014) Prognostic value of quantitative contrast-enhanced cardiovascular magnetic resonance for the evaluation of sudden death risk in patients with hypertrophic cardiomyopathy. Circulation 130(6):484–495

    Article  PubMed  Google Scholar 

  9. Choudary L, Mahrholdt H, Wagner A et al (2002) Myocardial scarring in asymptomatic or mildly symptomatic patients with hypertrophic cardiomyopathy. J Am Coll Cardiology 40:2156–2164

    Article  Google Scholar 

  10. Elias J Jr, dos Santos AC, Koenigkam-Santos M, Nogueira-Barbosa MH, Muglia VF (2008) Complications from the use of intravenous gadolinium-based contrast agents for magnetic resonance imaging. Radiol Bras 41(4):263–267

    Article  Google Scholar 

  11. Ennis DB, Epstein FH, Kellman P, Fananapazir L, McVeigh ER, Arai AE (2003) Assessment of regional systolic and diastolic dysfunction in familial hypertrophic cardiomyopathy using MR tagging. Magn Reson Med 50(3):638–642

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ganame J, Mertens L, Eidem BW, Claus P, D’Hooge J, Havemann LM, McMahon CJ, Elayda MA, Vaughn WK, Towbin JA, Ayres NA, Pignatelli RH (2007) Regional myocardial deformation in children with hypertrophic cardiomyopathy: morphologic and clinical correlations. Eur Heart J 28:2886–2894

    Article  PubMed  Google Scholar 

  13. Gersh BJ, Maron BJ, Bonow RO, Dearani JA, Fifer MA, Link MS, Naidu SS, Nishimura RA, Ommen SR, Rakowski H, Seidman CE, Towbin JA, Udelson JE, Yancy CW (2011) 2011 ACCF/AHA Guideline for the Diagnosis and Treatment of Hypertrophic Cardiomyopathy: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Developed in collaboration with the American Association for Thoracic Surgery, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. J Am Coll Cardiol 58:e212–e260

    Article  CAS  PubMed  Google Scholar 

  14. Gorcsan J 3rd, Tanaka H (2011) Echocardiographic assessment of myocardial strain. J Am Coll Cardiol 58(14):1401–1413

    Article  PubMed  Google Scholar 

  15. Greenberg NL, Firstenberg MS, Castro PL, Main M, Travaglini A, Odabashian JA, Drinko JK, Rodriquez LL, Thomas JD, Garcia MJ (2002) Doppler-derived myocardial systolic strain rate is a strong index of left ventricular contractility. Circulation 105(1):99–105

    Article  PubMed  Google Scholar 

  16. Hor KN, Gottliebson WM, Carson C, Wash E, Cnota J, Fleck R, Wansapura J, Klimeczek P, Al-Khalidi HR, Chung ES, Benson DW, Mazur W (2010) Comparison of magnetic resonance feature tracking for strain calculation with harmonic phase imaging analysis. JACC Cardiovasc Imaging 3(2):144–151

    Article  PubMed  Google Scholar 

  17. Hor KN, Baumann R, Pedrizzetti G, Tonti G, Gottliebson WM, Taylor M, Benson W, Mazur W (2011) Magnetic resonance derived myocardial strain assessment using feature tracking. J Vis Exp 48:2356–2361

    PubMed  Google Scholar 

  18. Kim YJ, Choi BW, Hur J, Lee HY, Seo JS, Kim TH, Choe KO, Ha JH (2008) Delayed enhancement in hypertrophic cardiomyopathy: comparison with myocardial tagging MRI. J Mag Reson Imaging 27(5):1054–1060

    Article  Google Scholar 

  19. Kowallick JT, Lamata P, Hussain ST, Kutty S, Steinmetz M, Sohns JM, Fasshauer M, Staab W, Unterberg-Buchwald C, Bigalke B, Lotz J, Hasenfub G, Schuster A (2014) Quantification of left ventricular torsion and diastolic recoil using cardiovascular magnetic resonance myocardial feature tracking. PLoS ONE 9:e109164

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kutty S, Rangamani S, Venkataraman J, Li L, Schuster A, Fletcher SE, Danford DA, Beerbaum P (2012) Reduced global longitudinal and radial strain with normal left ventricular ejection fraction late after effective repair of aortic coarctation: a CMR feature tracking study. Int J Cardiovasc Imaging 29:141–150

    Article  PubMed  Google Scholar 

  21. Lang SM, Shugh S, Mazur W, Sticka JJ, Rattan MS, Jefferies JL, Taylor MD (2015) Myocardial fibrosis and left ventricular dysfunction in Duchenne muscular dystrophy carriers using cardiac magnetic resonance imaging. Pediatr Cardiol 36(7):1495–1501. doi:10.1007/s00246-015-1192-7.

    Article  PubMed  Google Scholar 

  22. Maret E, Todt T, Brudin L, Nylander E, Swahn E, Ohlsson JL, Engvall JE (2009) Functional measurements based on feature tracking of cine magnetic resonance images identify left ventricular segments with myocardial scar. Cardiovasc Ultrasound 16(7):75. doi:10.1186/1476-7120-7-53

    Google Scholar 

  23. Maron BJ (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287:1308–1320

    PubMed  Google Scholar 

  24. Menon SC, Erickson LK, McFadden M, Miller DV (2013) Effect of ventriculotomy on right-ventricular remodeling in hypoplastic left heart syndrome: a histopathological and echocardiographic correlation study. Pediatr Cardiol 34(2):354–363

    Article  PubMed  Google Scholar 

  25. Moon JC, McKenna WJ, McCrohon JA, Elliott PM, Smith GC, Pennell DJ (2003) Toward clinical risk assessment in hypertrophic cardiomyopathy with gadolinium cardiovascular magnetic resonance. J Am Coll Cardiol 41:1561–1567

    Article  PubMed  Google Scholar 

  26. Morton G, Schuster A, Jogiya R, Kutty S, Beerbaum P, Nagel E (2012) Inter-study reproducibility of cardiovascular magnetic resonance myocardial feature tracking. J Cardiovasc Magn Reson 14:43

    Article  PubMed  PubMed Central  Google Scholar 

  27. O’Hanlon R, Grasso A, Roughton M, Moon JC, Clark S, Wage R, Webb J, Kulkarni M, Dawson D, Sulaibeekh L, Chandrasekaran B, Bucciarelli-Ducci C, Pasquale F, Cowie MR, McKenna WJ, Sheppard MN, Elliott PM, Pennell DJ, Prasad SK (2010) Prognostic significance of myocardial fibrosis in hypertrophic cardiomyopathy. J Am Coll Cardiol 56:867–874

    Article  PubMed  Google Scholar 

  28. Padiyath A, Gribben P, Abraham JR, Li L, Rangamani S, Schuster A, Dandord DA, Pedrizzetti G, Kutty S (2012) Echocardiography and cardiac magnetic resonance-based feature tracking in the assessment of myocardial mechanics in tetralogy of Fallot: an intermodality comparison. Echocardiography 30:203–210

    Article  PubMed  Google Scholar 

  29. Popovic ZB, Kwon DH, Mishra M, Buakhamsri A, Greenberg NL, Thamilarsan M, Flamm SD, Thomas JD, Lever HM, Desai MY (2008) Association between regional ventricular function and myocardial fibrosis in hypertrophic cardiomyopathy assessed by speckle tracking echocardiography and delayed hyperenhancement magnetic resonance imaging. J Am Soc Echocardiogr 21:1299–1305

    Article  PubMed  Google Scholar 

  30. Puchalski MD, Williams RV, Askovich B, Sower CT, Hor KH, Su JT, Pack N, Dibella E, Gottliebson WM (2009) Late gadolinium enhancement: precursor to cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiovasc Imaging 25(1):57–63

    Article  PubMed  PubMed Central  Google Scholar 

  31. Satio M, Okayama H, Yoshii T, Higashi H, Morioka H, Hiasa G, Sumimoto T, Inaba S, Nishimura K, Inoue K, Ogimoto A, Shigematsu Y, Hamada M, Higaki J (2012) Clinical significance of global two-dimensional strain as a surrogate parameter of myocardial fibrosis and cardiac events in patients with hypertrophic cardiomyopathy. Eur Heart J Cardiovasc Imaging 13:617–623

    Article  Google Scholar 

  32. Schuster A, Kutty S, Padiyath A, Parish V, Gribben P, Danford DA, Makowski MR, Bigalke B, Beerbaum P, Nagel E (2011) Cardiovascular magnetic resonance myocardial feature tracking detects quantitative wall motion during dobutamine stress. J Cardiovasc Magn Resonan 13:58

    Article  Google Scholar 

  33. Schuster A, Paul M, Bettencourt N, Morton G, Chiribiri A, Ishida M, Hussain S, Jogiya R, Kutty S, Bigalke B, Perera D, Nagel E (2013) Cardiovascular magnetic resonance myocardial feature tracking for quantitative viability assessment in ischemic cardiomyopathy. Int J Cardiol 166(2):413–420

    Article  PubMed  Google Scholar 

  34. Sengupta PP, Mehta V, Arora R, Mohan JC, Khandheria BK (2005) Quantification of regional nonuniformity and paradoxical intramural mechanics in hypertrophic cardiomyopathy by high frame rate ultrasound myocardial strain mapping. J Am Soc Echocardiogr 18:737–742

    Article  PubMed  Google Scholar 

  35. Serri K, Reant P, Lafitte M, Berhouet M, Bouffos VL, Roudaut R, Lafitte S (2006) Global and regional myocardial function quantification by two-dimensional strain. Application in hypertrophic cardiomyopathy. J Am Coll Cardiol 47(6):1175–1181

    Article  PubMed  Google Scholar 

  36. Shirani J, Pick R, Roberts WC, Maron BJ (2000) Morphology and significance of the left ventricular collagen network in young patients with hypertrophic cardiomyopathy and sudden cardiac death. J Am Coll Cardiology 35:36–44

    Article  CAS  Google Scholar 

  37. Smith BM, Dorfman AL, Yu S, Agarwal PP, Mahani MG, Lu JC (2007) Clinical significance of late gadolinium enhancement in pediatric patients with hypertrophic cardiomyopathy. Rev Esp Cardiol 60:15–23

    Article  Google Scholar 

  38. Smith BM, Dorfman AL, Yu S, Russell MW, Agarwal P, Mahani MG, Lu JC (2014) Clinical significance of late gadolinium enhancement in patients <20 years of age with hypertrophic cardiomyopathy. Am J Cardiol 113:1234–1239

    Article  PubMed  Google Scholar 

  39. Taylor RJ, Moody WE, Umar F, Edwards NC, Taylor TJ, Stegemann B, Townend JN, Hor KN, Steeds RP, Mazur W, Levya F (2015) Myocardial strain measurement with feature-tracking cardiovascular magnetic resonance: normal values. Eur Heart J Cardiovasc Imaging 16(8):871–881

    Article  PubMed  Google Scholar 

  40. Varnava AM, Elliott PM, Sharma S, Mckenna WJ, Davies MJ (2000) Hypertrophic cardiomyopathy: the interrelation of disarray, fibrosis, and small vessel disease. Heart 84:476–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Varnava AM, Elliott PM, Mahon N, Davies MJ, Mckenna WJ (2001) Relation between myocyte disarray and outcome in hypertrophic cardiomyopathy. Am J Cardiol 88:275–279

    Article  CAS  PubMed  Google Scholar 

  42. Weidemann F, Mertens L, Gewillig M, Sutherland GR (2001) Quantification of localized abnormal deformation in asymmetric nonobstructive hypertrophic cardiomyopathy: a velocity, strain rate, and strain Doppler myocardial imaging study. Pediatr Cardiol 22:534–537

    Article  CAS  PubMed  Google Scholar 

  43. Yang H, Sun JP, Lever HM, Popovic ZB, Drinko JK, Greenberg NL et al (2003) Use of strain imaging in detecting segmental dysfunction in patients with hypertrophic cardiomyopathy. J Am Soc Echocardiogr 16:233–239

    Article  PubMed  Google Scholar 

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Acknowledgments

This investigation was supported by the University of Utah Study Design and Biostatistics Center, with funding in part from the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant 8UL1TR000105 (formerly UL1RR025764).

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Correspondence to Shaji C. Menon.

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Bogarapu, S., Puchalski, M.D., Everitt, M.D. et al. Novel Cardiac Magnetic Resonance Feature Tracking (CMR-FT) Analysis for Detection of Myocardial Fibrosis in Pediatric Hypertrophic Cardiomyopathy. Pediatr Cardiol 37, 663–673 (2016). https://doi.org/10.1007/s00246-015-1329-8

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