Arrhythmic risk stratification by cardiac magnetic resonance tissue characterization: disclosing the arrhythmic substrate within the heart muscle

Abstract

Sudden cardiac death (SCD) is a pivotal health problem worldwide. The identification of subjects at increased risk of SCD is crucial for the accurate selection of candidates for implantable cardioverter defibrillator (ICD) therapy. Current strategies for arrhythmic stratification largely rely on left ventricular (LV) ejection fraction (EF), mostly measured by echocardiography, and New York Heart Association functional status for heart failure with reduced EF. For specific diseases, such as hypertrophic and arrhythmogenic cardiomyopathy, some risk scores have been proposed; however, these scores take into account some parameters that are a partial reflection of the global arrhythmic risk and show a suboptimal accuracy. Thanks to a more comprehensive evaluation, cardiac magnetic resonance (CMR) provides insights into the heart muscle (the so-called tissue characterization) identifying cardiac fibrosis as an arrhythmic substrate. Combining sequences before and after administration of contrast media and mapping techniques, CMR is able to characterize the myocardial tissue composition, shedding light on both intracellular and extracellular alterations. Over time, late gadolinium enhancement (LGE) emerged as solid prognostic marker, strongly associated with major arrhythmic events regardless of LVEF, adding incremental value over current strategy in ischemic heart disease and non-ischemic cardiomyopathies. The evidence on a potential prognostic role of mapping imaging is promising. However, mapping techniques require further investigation and standardization. Disclosing the arrhythmic substrate within the myocardium, CMR should be considered as part of a multiparametric approach to personalized arrhythmic stratification.

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

Fig. 1
Fig. 2

Data availability

Not applicable.

References

  1. 1.

    Tan HL, Dagres N, Böttiger BW, Schwartz PJ (2018) European Sudden Cardiac Arrest network: towards Prevention, Education and New Effective Treatments (ESCAPE-NET). Eur Heart J 39:86–88. https://doi.org/10.1093/eurheartj/ehx758

    Article  Google Scholar 

  2. 2.

    Priori SG, Blomstrom-Lundqvist C, Mazzanti A, Bloma N, Borggrefe M, Camm J, Elliott PM, Fitzsimons D, Hatala R, Hindricks G, Kirchhof P, Kjeldsen K, Kuck KH, Hernandez-Madrid A, Nikolaou N, Norekval TM, Spaulding C, Van Veldhuisen DJ, Kolh P, Lip GYH, Agewall S, Barón-Esquivias G, Boriani G, Budts W, Bueno H, Capodanno D, Carerj S, Crespo-Leiro MG, Czerny M, Deaton C, Dobrev D, Erol Ç, Galderisi M, Gorenek B, Kriebel T, Lambiase P, Lancellotti P, Lane DA, Lang I, Manolis AJ, Morais J, Moreno J, Piepoli MF, Rutten FH, Sredniawa B, Zamorano JL, Zannad F, Aboyans V, Achenbach S, Badimon L, Baumgartner H, Bax JJ, Dean V, Fitzsimons D, Gaemperli O, Nihoyannopoulos P, Ponikowski P, Roffi M, Torbicki A, Vaz Carneiro A, Windecker S, Piruzyan A, Roithinger FX, Mairesse GH, Goronja B, Shalganov T, Puljević D, Antoniades L, Kautzner J, Larsen JM, Aboulmaaty M, Kampus P, Hedman A, Kamcevska-Dobrkovic L, Piot O, Etsadashvili K, Eckardt L, Deftereos S, Gellér L, Gizurarson S, Keane D, Haim M, Della Bella P, Abdrakhmanov A, Mirrakhimov A, Kalejs O, Ben Lamin H, Marinskis G, Groben L, Sammut M, Raducan A, Chaib A, Tande PM, Lenarczyk R, Morgado FB, Vatasescu R, Mikhaylov EN, Hlivak P, Arenal A, Jensen-Urstad M, Sticherling C, Zeppenfeld K, Chettaoui R, Demir M, Duncan E, Parkhomenko A (2015) 2015 ESC guidelines for the management of patients with ventricular arrhythmias and the prevention of sudden cardiac death the task force for the Management of Patients with ventricular arrhythmias and the prevention of sudden cardiac death of the European Society of Cardiology (ESC). Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC). Eur Heart J. https://doi.org/10.1093/eurheartj/ehv316

  3. 3.

    J.J. Goldberger, M.E. Cain, S.H. Hohnloser, A.H. Kadish, B.P. Knight, M.S. Lauer, B.J. Maron, R.L. Page, R.S. Passman, D. Siscovick, W.G. Stevenson, D.P. Zipes, American Heart Association/American College of Cardiology Foundation/Heart Rhythm Society scientific statement on noninvasive risk stratification techniques for identifying patients at risk for sudden cardiac death: a scientific statement from the America, Circulation. (2008). doi:https://doi.org/10.1161/CIRCULATIONAHA.107.189375

  4. 4.

    Corrado D, Basso C, Pavei A, Michieli P, Schiavon M, Thiene G (2006) Trends in sudden cardiovascular death in young competitive athletes after implementation of a preparticipation screening program. J Am Med Assoc. https://doi.org/10.1001/jama.296.13.1593

  5. 5.

    Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, Falk V, Gonzalez-Juanatey JR, Harjola V-P, Jankowska EA, Jessup M, Linde C, Nihoyannopoulos P, Parissis JT, Pieske B, Riley JP, Rosano GMC, Ruilope LM, Ruschitzka F, Rutten FH, van der Meer P (2016) 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC). Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J 37:2129–2200. https://doi.org/10.1093/eurheartj/ehw128

    Article  Google Scholar 

  6. 6.

    Elliott PM, Anastasakis A, Borger MA, Borggrefe M, Cecchi F, Charron P, Hagege AA, Lafont A, Limongelli G, Mahrholdt H, McKenna WJ, Mogensen J, Nihoyannopoulos P, Nistri S, Pieper PG, Pieske B, Rapezzi C, Rutten FH, Tillmanns C, Watkins H (2014) European Society of Cardiology Guidelines on diagnosis and management of hypertrophic cardiomyopathy. Eur Heart J

  7. 7.

    Towbin JA, McKenna WJ, Abrams DJ, Ackerman MJ, Calkins H, Darrieux FCC, Daubert JP, de Chillou C, DePasquale EC, Desai MY, Estes NAM, Hua W, Indik JH, Ingles J, James CA, John RM, Judge DP, Keegan R, Krahn AD, Link MS, Marcus FI, McLeod CJ, Mestroni L, Priori SG, Saffitz JE, Sanatani S, Shimizu W, van Tintelen JP, Wilde AAM, Zareba W (2019) 2019 HRS expert consensus statement on evaluation, risk stratification, and management of arrhythmogenic cardiomyopathy. Hear, Rhythm. https://doi.org/10.1016/j.hrthm.2019.05.007

    Google Scholar 

  8. 8.

    Lang RM, Badano LP, Victor MA, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Retzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. https://doi.org/10.1016/j.echo.2014.10.003

  9. 9.

    Pocock SJ, Ariti CA, McMurray JJV, Maggioni A, Køber L, Squire IB, Swedberg K, Dobson J, Poppe KK, Whalley GA, Doughty RN (2013) Predicting survival in heart failure: a risk score based on 39 372 patients from 30 studies. Eur Heart J. https://doi.org/10.1093/eurheartj/ehs337

  10. 10.

    Køber L, Thune JJ, Nielsen JC, Haarbo J, Videbæk L, Korup E, Jensen G, Hildebrandt P, Steffensen FH, Bruun NE, Eiskjær H, Brandes A, Thøgersen AM, Gustafsson F, Egstrup K, Videbæk R, Hassager C, Svendsen JH, Høfsten DE, Torp-Pedersen C, Pehrson S (2016) Defibrillator implantation in patients with nonischemic systolic heart failure. N Engl J Med 375:1221–1230. https://doi.org/10.1056/NEJMoa1608029

    Article  Google Scholar 

  11. 11.

    M. Merlo, P. Gentile, J. Artico, A. Cannatà, A. Paldino, G. De Angelis, G. Barbati, M. Alonge, M. Gigli, B. Pinamonti, F. Ramani, M. Zecchin, F. Pirozzi, D. Stolfo, G. Sinagra, Arrhythmic risk stratification in patients with dilated cardiomyopathy and intermediate left ventricular dysfunction, J. Cardiovasc. Med. (Hagerstown). (2019). doi:https://doi.org/10.2459/JCM.0000000000000792

  12. 12.

    Vaduganathan M, Michel A, Hall K, Mulligan C, Nodari S, Shah SJ, Senni M, Triggiani M, Butler J, Gheorghiade M (2016) Spectrum of epidemiological and clinical findings in patients with heart failure with preserved ejection fraction stratified by study design: a systematic review. Eur J Heart Fail. https://doi.org/10.1002/ejhf.442

  13. 13.

    M.R. Zile, W.H. Gaasch, I.S. Anand, M. Haass, W.C. Little, A.B. Miller, J. Lopez-Sendon, J.R. Teerlink, M. White, J.J. McMurray, M. Komajda, R. McKelvie, A. Ptaszynska, S.J. Hetzel, B.M. Massie, P.E. Carson, Mode of death in patients with heart failure and a preserved ejection fraction: results from the irbesartan in heart failure with preserved ejection fraction study (I-Preserve) Trial, Circulation. (2010). doi:https://doi.org/10.1161/CIRCULATIONAHA.109.909614

  14. 14.

    Mele D, Nardozza M, Ferrari R (2018) Left ventricular ejection fraction and heart failure: an indissoluble marriage? Eur J Heart Fail. https://doi.org/10.1002/ejhf.1071

  15. 15.

    M.A. Konstam, F.M. Abboud, Ejection fraction: misunderstood and overrated (changing the paradigm in categorizing heart failure), Circulation. (2017). doi:https://doi.org/10.1161/CIRCULATIONAHA.116.025795

  16. 16.

    G. Pontone, A.I. Guaricci, D. Andreini, A. Solbiati, M. Guglielmo, S. Mushtaq, A. Baggiano, V. Beltrama, L. Fusini, C. Rota, C. Segurini, E. Conte, P. Gripari, A. Dello Russo, M. Moltrasio, F. Tundo, F. Lombardi, G. Muscogiuri, V. Lorenzoni, C. Tondo, P. Agostoni, A.L. Bartorelli, M. Pepi, Prognostic benefit of cardiac magnetic resonance over transthoracic echocardiography for the assessment of ischemic and nonischemic dilated cardiomyopathy patients referred for the evaluation of primary prevention implantable cardioverter-defibrillator therapy, Circ. Cardiovasc. Imaging. (2016). doi:https://doi.org/10.1161/CIRCIMAGING.115.004956

  17. 17.

    Jenkins C, Moir S, Chan J, Rakhit D, Haluska B, Marwick TH (2009) Left ventricular volume measurement with echocardiography: a comparison of left ventricular opacification, three-dimensional echocardiography, or both with magnetic resonance imaging. Eur Heart J. https://doi.org/10.1093/eurheartj/ehn484

  18. 18.

    P.A. Pellikka, L. She, T.A. Holly, G. Lin, P. Varadarajan, R.G. Pai, R.O. Bonow, G.M. Pohost, J.A. Panza, D.S. Berman, D.L. Prior, F.M. Asch, S. Borges-Neto, P. Grayburn, H.R. Al-Khalidi, K. Miszalski-Jamka, P. Desvigne-Nickens, K.L. Lee, E.J. Velazquez, J.K. Oh, Variability in ejection fraction measured by echocardiography, gated single-photon emission computed tomography, and cardiac magnetic resonance in patients with coronary artery disease and left ventricular dysfunction, JAMA Netw. Open. (2018). doi:https://doi.org/10.1001/jamanetworkopen.2018.1456

  19. 19.

    de Haan S, de Boer K, Commandeur J, Beek AM, van Rossum AC, Allaart CP (2014) Assessment of left ventricular ejection fraction in patients eligible for ICD therapy: discrepancy between cardiac magnetic resonance imaging and 2D echocardiography. Netherlands Hear J. https://doi.org/10.1007/s12471-014-0594-0

  20. 20.

    Joshi SB, Connelly KA, Jimenez-Juan L, Hansen M, Kirpalani A, Dorian P, Mangat I, Al-Hesayen A, Crean AM, Wright GA, Yan AT, Leong-Poi H (2012) Potential clinical impact of cardiovascular magnetic resonance assessment of ejection fraction on eligibility for cardioverter defibrillator implantation. J Cardiovasc Magn Reson. https://doi.org/10.1186/1532-429X-14-69

  21. 21.

    F. Contijoch, K. Rogers, H. Rears, M. Shahid, P. Kellman, J. Gorman, R.C. Gorman, P. Yushkevich, E.S. Zado, G.E. Supple, F.E. Marchlinski, W.R.T. Witschey, Y. Han, Quantification of left ventricular function with premature ventricular complexes reveals variable hemodynamics, Circ. Arrhythmia Electrophysiol. 9 (2016). doi:https://doi.org/10.1161/CIRCEP.115.003520

  22. 22.

    Akhtari S, Chuang ML, Salton CJ, Berg S, Kissinger KV, Goddu B, O’Donnell CJ, Manning WJ (2018) Effect of isolated left bundle-branch block on biventricular volumes and ejection fraction: a cardiovascular magnetic resonance assessment. J Cardiovasc Magn Reson 20:66. https://doi.org/10.1186/s12968-018-0457-8

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    N.S. Peters, A.L. Wit, Myocardial architecture and ventricular arrhythmogenesis, Circulation. (1998). doi:https://doi.org/10.1161/01.CIR.97.17.1746

  24. 24.

    Di Marco A, Anguera I, Schmitt M, Klem I, Neilan TG, White JA, Sramko M, Masci PG, Barison A, Mckenna P, Mordi I, Haugaa KH, Leyva F, Rodriguez Capitán J, Satoh H, Nabeta T, Dallaglio PD, Campbell NG, Sabaté X, Cequier Á (2017) Late gadolinium enhancement and the risk for ventricular arrhythmias or sudden death in dilated cardiomyopathy. JACC Hear Fail 5:28–38. https://doi.org/10.1016/j.jchf.2016.09.017

    Article  Google Scholar 

  25. 25.

    Disertori M, Rigoni M, Pace N, Casolo G, Masè M, Gonzini L, Lucci D, Nollo G, Ravelli F (2016) Myocardial fibrosis assessment by LGE is a powerful predictor of ventricular tachyarrhythmias in ischemic and nonischemic LV dysfunction: a meta-analysis. JACC Cardiovasc, Imaging. https://doi.org/10.1016/j.jcmg.2016.01.033

    Google Scholar 

  26. 26.

    Ganesan AN, Gunton J, Nucifora G, McGavigan AD, Selvanayagam JB (2018) Impact of late gadolinium enhancement on mortality, sudden death and major adverse cardiovascular events in ischemic and nonischemic cardiomyopathy: a systematic review and meta-analysis. Int J Cardiol. https://doi.org/10.1016/j.ijcard.2017.10.094

  27. 27.

    V.O. Puntmann, T. Voigt, Z. Chen, M. Mayr, R. Karim, K. Rhode, A. Pastor, G. Carr-White, R. Razavi, T. Schaeffter, E. Nagel, Native T1 mapping in differentiation of normal myocardium from diffuse disease in hypertrophic and dilated cardiomyopathy., JACC. Cardiovasc. Imaging. 6 (2013) 475–484. doi:https://doi.org/10.1016/j.jcmg.2012.08.019

  28. 28.

    D.R. Messroghli, J.C. Moon, V.M. Ferreira, L. Grosse-Wortmann, T. He, P. Kellman, J. Mascherbauer, R. Nezafat, M. Salerno, E.B. Schelbert, A.J. Taylor, R. Thompson, M. Ugander, R.B. Van Heeswijk, M.G. Friedrich, Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2 and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI), J. Cardiovasc. Magn. Reson. (2017). doi:https://doi.org/10.1186/s12968-017-0389-8

  29. 29.

    Iles LM, Ellims AH, Llewellyn H, Hare JL, Kaye DM, McLean CA, Taylor AJ (2015) Histological validation of cardiac magnetic resonance analysis of regional and diffuse interstitial myocardial fibrosis. Eur. Heart J. Cardiovasc, Imaging. https://doi.org/10.1093/ehjci/jeu182

    Google Scholar 

  30. 30.

    P. Thavendiranathan, M. Walls, S. Giri, D. Verhaert, S. Rajagopalan, S. Moore, O.P. Simonetti, S. V Raman, Improved detection of myocardial involvement in acute inflammatory cardiomyopathies using T2 mapping., Circ. Cardiovasc. Imaging. 5 (2012) 102–110. doi:https://doi.org/10.1161/CIRCIMAGING.111.967836

  31. 31.

    Lurz JA, Luecke C, Lang D, Besler C, Rommel K-P, Klingel K, Kandolf R, Adams V, Schöne K, Hindricks G, Schuler G, Linke A, Thiele H, Gutberlet M, Lurz P (2018) CMR–derived extracellular volume fraction as a marker for myocardial fibrosis. JACC Cardiovasc Imaging 11:38–45. https://doi.org/10.1016/j.jcmg.2017.01.025

    Article  Google Scholar 

  32. 32.

    Vita T, Gräni C, Abbasi SA, Neilan TG, Rowin E, Kaneko K, Coelho-Filho O, Watanabe E, Mongeon F-P, Farhad H, Rassi CH, Choi YL, Cheng K, Givertz MM, Blankstein R, Steigner M, Aghayev A, Jerosch-Herold M, Kwong RY (2019) Comparing CMR mapping methods and myocardial patterns toward heart failure outcomes in nonischemic dilated cardiomyopathy. JACC Cardiovasc Imaging 12:1659–1669. https://doi.org/10.1016/j.jcmg.2018.08.021

    Article  PubMed  Google Scholar 

  33. 33.

    Miller CA, Naish JH, Bishop P, Coutts G, Clark D, Zhao S, Ray SG, Yonan N, Williams SG, Flett AS, Moon JC, Greiser A, Parker GJM, Schmitt M (2013) Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circ. Cardiovasc. Imaging. 6:373–383. https://doi.org/10.1161/CIRCIMAGING.112.000192

    Article  PubMed  Google Scholar 

  34. 34.

    Barison A, Grigoratos C, Todiere G, Aquaro GD (2015) Myocardial interstitial remodelling in non-ischaemic dilated cardiomyopathy: insights from cardiovascular magnetic resonance. Heart Fail Rev 20:731–749. https://doi.org/10.1007/s10741-015-9509-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Selvanayagam JB, Hartshorne T, Billot L, Grover S, Hillis GS, Jung W, Krum H, Prasad S, McGavigan AD (2017) Cardiovascular magnetic resonance-GUIDEd management of mild to moderate left ventricular systolic dysfunction (CMR GUIDE): study protocol for a randomized controlled trial. Ann Noninvasive Electrocardiol. https://doi.org/10.1111/anec.12420

  36. 36.

    McCrohon JA, Moon JCC, Prasad SK, McKenna WJ, Lorenz CH, Coats AJS, Pennell DJ (2003) Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation. 108:54–59. https://doi.org/10.1161/01.CIR.0000078641.19365.4C

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Soriano CJ, Ridocci F, Estornell J, Jimenez J, Martinez V, De Velasco JA (2005) Noninvasive diagnosis of coronary artery disease in patients with heart failure and systolic dysfunction of uncertain etiology, using late gadolinium-enhanced cardiovascular magnetic resonance. J Am Coll Cardiol 45:743–748. https://doi.org/10.1016/j.jacc.2004.11.037

    Article  PubMed  Google Scholar 

  38. 38.

    A.T. Yan, A.J. Shayne, K.A. Brown, S.N. Gupta, C.W. Chan, T.M. Luu, M.F. Di Carli, H.G. Reynolds, W.G. Stevenson, R.Y. Kwong, Characterization of the peri-infarct zone by contrast-enhanced cardiac magnetic resonance imaging is a powerful predictor of post-myocardial infarction mortality, Circulation. (2006). doi:https://doi.org/10.1161/CIRCULATIONAHA.106.613414

  39. 39.

    A. Schmidt, C.F. Azevedo, A. Cheng, S.N. Gupta, D.A. Bluemke, T.K. Foo, G. Gerstenblith, R.G. Weiss, E. Marbán, G.F. Tomaselli, J.A.C. Lima, K.C. Wu, Infarct tissue heterogeneity by magnetic resonance imaging identifies enhanced cardiac arrhythmia susceptibility in patients with left ventricular dysfunction, Circulation. (2007). doi:https://doi.org/10.1161/CIRCULATIONAHA.106.653568

  40. 40.

    Jablonowski R, Chaudhry U, Van Der Pals J, Engblom H, Arheden H, Heiberg E, Wu KC, Borgquist R, Carlsson M (2017) Cardiovascular magnetic resonance to predict appropriate implantable cardioverter defibrillator therapy in ischemic and nonischemic cardiomyopathy patients using late gadolinium enhancement border zone comparison of four analysis methods. Circ. Cardiovasc, Imaging. https://doi.org/10.1161/CIRCIMAGING.116.006105

    Google Scholar 

  41. 41.

    Watanabe E, Abbasi SA, Heydari B, Coelho-Filho OR, Shah R, Neilan TG, Murthy VL, Mongeon F-P, Barbhaiya C, Jerosch-Herold M, Blankstein R, Hatabu H, van der Geest RJ, Stevenson WG, Kwong RY (2014) Infarct tissue heterogeneity by contrast-enhanced magnetic resonance imaging is a novel predictor of mortality in patients with chronic coronary artery disease and left ventricular dysfunction. Circ Cardiovasc Imaging 7:887–894. https://doi.org/10.1161/CIRCIMAGING.113.001293

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    J. Acosta, J. Fernández-Armenta, R. Borràs, I. Anguera, F. Bisbal, J. Martí-Almor, J.M. Tolosana, D. Penela, D. Andreu, D. Soto-Iglesias, R. Evertz, M. Matiello, C. Alonso, R. Villuendas, T.M. de Caralt, R.J. Perea, J.T. Ortiz, X. Bosch, L. Serra, X. Planes, A. Greiser, O. Ekinci, L. Lasalvia, L. Mont, A. Berruezo, Scar characterization to predict life-threatening arrhythmic events and sudden cardiac death in patients with cardiac resynchronization therapy, JACC Cardiovasc. Imaging. 11 (2018) 561–572. doi:https://doi.org/10.1016/j.jcmg.2017.04.021

  43. 43.

    Z. Chen, M. Sohal, T. Voigt, E. Sammut, C. Tobon-Gomez, N. Child, T. Jackson, A. Shetty, J. Bostock, M. Cooklin, M. O’Neill, M. Wright, F. Murgatroyd, J. Gill, G. Carr-White, A. Chiribiri, T. Schaeffter, R. Razavi, C.A. Rinaldi, Myocardial tissue characterization by cardiac magnetic resonance imaging using T1 mapping predicts ventricular arrhythmia in ischemic and non-ischemic cardiomyopathy patients with implantable cardioverter-defibrillators, Hear. Rhythm. (2015). doi:https://doi.org/10.1016/j.hrthm.2014.12.020

  44. 44.

    G. Pontone, A.I. Guaricci, D. Andreini, G. Ferro, M. Guglielmo, A. Baggiano, L. Fusini, G. Muscogiuri, V. Lorenzoni, S. Mushtaq, E. Conte, A. Annoni, A. Formenti, M.E. Mancini, P. Carità, M. Verdecchia, S. Pica, F. Fazzari, N. Cosentino, G. Marenzi, M.G. Rabbat, P. Agostoni, A.L. Bartorelli, M. Pepi, P.G. Masci, Prognostic stratification of patients with ST-segment-elevation myocardial infarction (PROSPECT): a cardiac magnetic resonance study, Circ. Cardiovasc. Imaging. (2017). doi:https://doi.org/10.1161/CIRCIMAGING.117.006428

  45. 45.

    Stone GW, Selker HP, Thiele H, Patel MR, Udelson JE, Ohman EM, Maehara A, Eitel I, Granger CB, Jenkins PL, Nichols M, Ben-Yehuda O (2016) Relationship between infarct size and outcomes following primary PCI patient-level analysis from 10 randomized trials. J Am Coll Cardiol. https://doi.org/10.1016/j.jacc.2016.01.069

  46. 46.

    Izquierdo M, Ruiz-Granell R, Bonanad C, Chaustre F, Gomez C, Ferrero A, Lopez-Lereu P, Monmeneu JV, Nuñez J, Chorro FJ, Bodi V (2013) Value of early cardiovascular magnetic resonance for the prediction of adverse arrhythmic cardiac events after a first noncomplicated ST-segment-elevation myocardial infarction. Circ. Cardiovasc, Imaging. https://doi.org/10.1161/CIRCIMAGING.113.000702

    Google Scholar 

  47. 47.

    Carrick D, Haig C, Rauhalammi S, Ahmed N, Mordi I, McEntegart M, Petrie MC, Eteiba H, Hood S, Watkins S, Lindsay M, Mahrous A, Ford I, Tzemos N, Sattar N, Welsh P, Radjenovic A, Oldroyd KG, Berry C (2016) Prognostic significance of infarct core pathology revealed by quantitative non-contrast in comparison with contrast cardiac magnetic resonance imaging in reperfused ST-elevation myocardial infarction survivors. Eur Heart J. https://doi.org/10.1093/eurheartj/ehv372

  48. 48.

    Kidambi A, Motwani M, Uddin A, Ripley DP, McDiarmid AK, Swoboda PP, Broadbent DA, Al Musa T, Erhayiem B, Leader J, Croisille P, Clarysse P, Greenwood JP, Plein S (2017) Myocardial extracellular volume estimation by CMR predicts functional recovery following acute MI. JACC Cardiovasc, Imaging. https://doi.org/10.1016/j.jcmg.2016.06.015

    Google Scholar 

  49. 49.

    Baroldi G, Silver MD, De Maria R, Parodi O, Pellegrini A (1997) Lipomatous metaplasia in left ventricular scar. Can J Cardiol 13:65–71 http://www.ncbi.nlm.nih.gov/pubmed/9039067

    CAS  PubMed  Google Scholar 

  50. 50.

    Mordi I, Radjenovic A, Stanton T, Gardner RS, McPhaden A, Carrick D, Berry C, Tzemos N (2015) Prevalence and prognostic significance of lipomatous metaplasia in patients with prior myocardial infarction. JACC Cardiovasc Imaging 8:1111–1112. https://doi.org/10.1016/j.jcmg.2014.07.024

    Article  PubMed  Google Scholar 

  51. 51.

    Pouliopoulos J, Chik WWB, Kanthan A, Sivagangabalan G, Barry MA, Fahmy PNA, Midekin C, Lu J, Kizana E, Thomas SP, Thiagalingam A, Kovoor P (2013) Intramyocardial adiposity after myocardial infarction. Circulation. 128:2296–2308. https://doi.org/10.1161/CIRCULATIONAHA.113.002238

    Article  PubMed  Google Scholar 

  52. 52.

    Merlo M, Cannata A, Gobbo M, Stolfo D, Elliott PM, Sinagra G (2018) Evolving concepts in dilated cardiomyopathy. Eur J Heart Fail 20:228–239. https://doi.org/10.1002/ejhf.1103

    Article  PubMed  Google Scholar 

  53. 53.

    Merlo M, Caiffa T, Gobbo M, Adamo L, Sinagra G (2018) Reverse remodeling in dilated cardiomyopathy: insights and future perspectives. IJC Hear Vasc 18:52–57. https://doi.org/10.1016/j.ijcha.2018.02.005

    CAS  Article  Google Scholar 

  54. 54.

    Porcari A, De Angelis G, Romani S, Paldino A, Artico J, Cannatà A, Gentile P, Pinamonti B, Merlo M, Sinagra G (2019) Current diagnostic strategies for dilated cardiomyopathy: a comparison of imaging techniques. Expert Rev. Cardiovasc, Ther. https://doi.org/10.1080/14779072.2019.1550719

    Google Scholar 

  55. 55.

    Zecchin M, Merlo M, Pivetta A, Barbati G, Lutman C, Gregori D, Serdoz LV, Bardari S, Magnani S, Di Lenarda A, Proclemer A, Sinagra G (2012) How can optimization of medical treatment avoid unnecessary implantable cardioverter-defibrillator implantations in patients with idiopathic dilated cardiomyopathy presenting with “sCD-HeFT Criteria?,”. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2011.10.033

  56. 56.

    Losurdo P, Stolfo D, Merlo M, Barbati G, Gobbo M, Gigli M, Ramani F, Pinamonti B, Zecchin M, Finocchiaro G, Mestroni L, Sinagra G (2016) Early arrhythmic events in idiopathic dilated cardiomyopathy. JACC Clin, Electrophysiol. https://doi.org/10.1016/j.jacep.2016.05.002

    Google Scholar 

  57. 57.

    Gulati A, Jabbour A, Ismail TF, Guha K, Khwaja J, Raza S, Morarji K, Brown TDH, Ismail NA, Dweck MR, Di Pietro E, Roughton M, Wage R, Daryani Y, O’Hanlon R, Sheppard MN, Alpendurada F, Lyon AR, Cook SA, Cowie MR, Assomull RG, Pennell DJ, Prasad SK (2013) Association of fibrosis with mortality and sudden cardiac death in patients with nonischemic dilated cardiomyopathy. JAMA - J. Am. Med, Assoc. https://doi.org/10.1001/jama.2013.1363

    Google Scholar 

  58. 58.

    Halliday BP, Cleland JGF, Goldberger JJ, Prasad SK (2017) Personalizing risk stratification for sudden death in dilated cardiomyopathy. Circulation. 136:215–231. https://doi.org/10.1161/CIRCULATIONAHA.116.027134

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Iles L, Pfluger H, Lefkovits L, Butler MJ, Kistler PM, Kaye DM, Taylor AJ (2011) Myocardial fibrosis predicts appropriate device therapy in patients with implantable cardioverter-defibrillators for primary prevention of sudden cardiac death. J Am Coll Cardiol 57:821–828. https://doi.org/10.1016/j.jacc.2010.06.062

    Article  PubMed  Google Scholar 

  60. 60.

    B.P. Halliday, A. Gulati, A. Ali, K. Guha, S. Newsome, M. Arzanauskaite, V.S. Vassiliou, A. Lota, C. Izgi, U. Tayal, Z. Khalique, C. Stirrat, D. Auger, N. Pareek, T.F. Ismail, S.D. Rosen, A. Vazir, F. Alpendurada, J. Gregson, M.P. Frenneaux, M.R. Cowie, J.G.F. Cleland, S.A. Cook, D.J. Pennell, S.K. Prasad, Association between midwall late gadolinium enhancement and sudden cardiac death in patients with dilated cardiomyopathy and mild and moderate left ventricular systolic dysfunction., Circulation. 135 (2017) 2106–2115. doi:https://doi.org/10.1161/CIRCULATIONAHA.116.026910

  61. 61.

    S. Nazarian, D.A. Bluemke, A.C. Lardo, M.M. Zviman, S.P. Watkins, T.L. Dickfeld, G.R. Meininger, A. Roguin, H. Calkins, G.F. Tomaselli, R.G. Weiss, R.D. Berger, J.A.C. Lima, H.R. Halperin, Magnetic resonance assessment of the substrate for inducible ventricular tachycardia in nonischemic cardiomyopathy, Circulation. (2005). doi:https://doi.org/10.1161/CIRCULATIONAHA.105.549659

  62. 62.

    Sasaki T, Miller CF, Hansford R, Zipunnikov V, Zviman MM, Marine JE, Spragg D, Cheng A, Tandri H, Sinha S, Kolandaivelu A, Zimmerman SL, Bluemke DA, Tomaselli GF, Berger RD, Halperin HR, Calkins H, Nazarian S (2013) Impact of nonischemic scar features on local ventricular electrograms and scar-related ventricular tachycardia circuits in patients with nonischemic cardiomyopathy. Circ, Arrhythmia Electrophysiol. https://doi.org/10.1161/CIRCEP.113.000159

    Google Scholar 

  63. 63.

    Marume K, Noguchi T, Tateishi E, Morita Y, Kamakura T, Ishibashi K, Noda T, Miura H, Nishimura K, Nakai M, Yamada N, Tsujita K, Anzai T, Kusano K, Ogawa H, Yasuda S (2018) Mortality and sudden cardiac death risk stratification using the noninvasive combination of wide QRS duration and late gadolinium enhancement in idiopathic dilated cardiomyopathy. Circ, Arrhythmia Electrophysiol. https://doi.org/10.1161/CIRCEP.117.006233

    Google Scholar 

  64. 64.

    Elming MB, Hammer-Hansen S, Voges I, Nyktari E, Raja AA, Svendsen JH, Pehrson S, Signorovitch J, Køber L, Prasad SK, Thune JJ (2019) Myocardial fibrosis and the effect of primary prophylactic defibrillator implantation in patients with non-ischemic systolic heart failure—DANISH-MRI. Am Heart J. https://doi.org/10.1016/j.ahj.2019.10.020

  65. 65.

    Kalra R, Shenoy C (2019) Identifying nonischemic cardiomyopathy patients who would benefit from an implantable cardioverter-defibrillator: can late gadolinium enhancement on cardiovascular magnetic resonance imaging help? Am Heart J. https://doi.org/10.1016/j.ahj.2019.12.010

  66. 66.

    Gutman SJ, Costello BT, Papapostolou S, Voskoboinik A, Iles L, Ja J, Hare JL, Ellims A, Kistler PM, Marwick TH, Taylor AJ (2019) Reduction in mortality from implantable cardioverter-defibrillators in non-ischaemic cardiomyopathy patients is dependent on the presence of left ventricular scar. Eur Heart J. https://doi.org/10.1093/eurheartj/ehy437

  67. 67.

    Halliday BP, Baksi AJ, Gulati A, Ali A, Newsome S, Izgi C, Arzanauskaite M, Lota A, Tayal U, Vassiliou VS, Gregson J, Alpendurada F, Frenneaux MP, Cook SA, Cleland JGF, Pennell DJ, Prasad SK (2018) Outcome in dilated cardiomyopathy related to the extent, location, and pattern of late gadolinium enhancement. JACC Cardiovasc, Imaging. https://doi.org/10.1016/j.jcmg.2018.07.015

    Google Scholar 

  68. 68.

    Puntmann VO, Carr-White G, Jabbour A, Yu CY, Gebker R, Kelle S, Hinojar R, Doltra A, Varma N, Child N, Rogers T, Suna G, Arroyo Ucar E, Goodman B, Khan S, Dabir D, Herrmann E, Zeiher AM, Nagel E (2016) T1-mapping and outcome in nonischemic cardiomyopathy all-cause mortality and heart failure. JACC Cardiovasc, Imaging. https://doi.org/10.1016/j.jcmg.2015.12.001

    Google Scholar 

  69. 69.

    Nakamori S, Bui AH, Jang J, El-Rewaidy HA, Kato S, Ngo LH, Josephson ME, Manning WJ, Nezafat R (2018) Increased myocardial native T1 relaxation time in patients with nonischemic dilated cardiomyopathy with complex ventricular arrhythmia. J Magn Reson Imaging. https://doi.org/10.1002/jmri.25811

  70. 70.

    Nakamori S, Dohi K, Ishida M, Goto Y, Imanaka-Yoshida K, Omori T, Goto I, Kumagai N, Fujimoto N, Ichikawa Y, Kitagawa K, Yamada N, Sakuma H, Ito M (2018) Native T1 mapping and extracellular volume mapping for the assessment of diffuse myocardial fibrosis in dilated cardiomyopathy. JACC Cardiovasc, Imaging. https://doi.org/10.1016/j.jcmg.2017.04.006

    Google Scholar 

  71. 71.

    Paldino A, De Angelis G, Merlo M, Gigli M, Dal Ferro M, Severini GM, Mestroni L, Sinagra G (2018) Genetics of dilated cardiomyopathy: clinical implications. Curr Cardiol Rep. https://doi.org/10.1007/s11886-018-1030-7

  72. 72.

    A.L.P. Caforio, S. Pankuweit, E. Arbustini, C. Basso, J. Gimeno-Blanes, S.B. Felix, M. Fu, T. Helio, S. Heymans, R. Jahns, K. Klingel, A. Linhart, B. Maisch, W. McKenna, J. Mogensen, Y.M. Pinto, A. Ristic, H.-P. Schultheiss, H. Seggewiss, L. Tavazzi, G. Thiene, A. Yilmaz, P. Charron, P.M. Elliott, Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases., Eur. Heart J. 34 (2013) 2636–48, 2648a-2648d. doi:https://doi.org/10.1093/eurheartj/eht210

  73. 73.

    J.W. Mason, J.B. O’Connell, A. Herskowitz, N.R. Rose, B.M. McManus, M.E. Billingham, T.E. Moon, A clinical trial of immunosuppressive therapy for myocarditis. The Myocarditis Treatment Trial Investigators., N. Engl. J. Med. (1995). doi:https://doi.org/10.1056/NEJM199508033330501

  74. 74.

    Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, White JA, Abdel-Aty H, Gutberlet M, Prasad S, Aletras A, Laissy J-P, Paterson I, Filipchuk NG, Kumar A, Pauschinger M, Liu P (2009) Cardiovascular magnetic resonance in myocarditis: a JACC White paper. J Am Coll Cardiol 53:1475–1487. https://doi.org/10.1016/j.jacc.2009.02.007

    Article  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Grun S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, Kispert E-M, Hill S, Ong P, Klingel K, Kandolf R, Sechtem U, Mahrholdt H (2012) Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery. J Am Coll Cardiol 59:1604–1615. https://doi.org/10.1016/j.jacc.2012.01.007

    Article  PubMed  Google Scholar 

  76. 76.

    Gräni C, Eichhorn C, Bière L, Murthy VL, Agarwal V, Kaneko K, Cuddy S, Aghayev A, Steigner M, Blankstein R, Jerosch-Herold M, Kwong RY (2017) Prognostic value of cardiac magnetic resonance tissue characterization in risk stratifying patients with suspected myocarditis. J Am Coll Cardiol. https://doi.org/10.1016/j.jacc.2017.08.050

  77. 77.

    G.D. Aquaro, M. Perfetti, G. Camastra, L. Monti, S. Dellegrottaglie, C. Moro, A. Pepe, G. Todiere, C. Lanzillo, A. Scatteia, M. Di Roma, G. Pontone, M. Perazzolo Marra, A. Barison, G. Di Bella, Cardiac MR with late gadolinium enhancement in acute myocarditis with preserved systolic function: ITAMY Study, J. Am. Coll. Cardiol. 70 (2017) 1977–1987. doi:https://doi.org/10.1016/j.jacc.2017.08.044

  78. 78.

    Sinagra G, Anzini M, Pereira NL, Bussani R, Finocchiaro G, Bartunek J, Merlo M (2016) Myocarditis in clinical practice. Mayo Clin Proc 91:1256–1266. https://doi.org/10.1016/j.mayocp.2016.05.013

    Article  PubMed  Google Scholar 

  79. 79.

    Peretto G, Sala S, Rizzo S, Palmisano A, Esposito A, De Cobelli F, Campochiaro C, De Luca G, Foppoli L, Dagna L, Thiene G, Basso C, Della Bella P (2020) Ventricular arrhythmias in myocarditis. J Am Coll Cardiol 75:1046–1057. https://doi.org/10.1016/j.jacc.2020.01.036

    Article  PubMed  Google Scholar 

  80. 80.

    Anzini M, Merlo M, Artico J, Sinagra G (2016) Arrhythmic risk prediction of acute myocarditis presenting with life-threatening ventricular tachyarrhythmias. Int J Cardiol 212:169–170. https://doi.org/10.1016/j.ijcard.2016.03.020

    Article  PubMed  Google Scholar 

  81. 81.

    Francone M, Chimenti C, Galea N, Scopelliti F, Verardo R, Galea R, Carbone I, Catalano C, Fedele F, Frustaci A (2014) CMR sensitivity varies with clinical presentation and extent of cell necrosis in biopsy-proven acute myocarditis. JACC Cardiovasc Imaging 7:254–263. https://doi.org/10.1016/j.jcmg.2013.10.011

    Article  PubMed  Google Scholar 

  82. 82.

    V.M. Ferreira, J. Schulz-Menger, G. Holmvang, C.M. Kramer, I. Carbone, U. Sechtem, I. Kindermann, M. Gutberlet, L.T. Cooper, P. Liu, M.G. Friedrich, Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations., J. Am. Coll. Cardiol. 72 (2018) 3158–3176. doi:https://doi.org/10.1016/j.jacc.2018.09.072

  83. 83.

    Spieker M, Haberkorn S, Gastl M, Behm P, Katsianos S, Horn P, Jacoby C, Schnackenburg B, Reinecke P, Kelm M, Westenfeld R, Bönner F (2017) Abnormal T2 mapping cardiovascular magnetic resonance correlates with adverse clinical outcome in patients with suspected acute myocarditis. J Cardiovasc Magn Reson. https://doi.org/10.1186/s12968-017-0350-x

  84. 84.

    J.A. Luetkens, R. Homsi, D. Dabir, D.L. Kuetting, C. Marx, J. Doerner, U. Schlesinger-Irsch, R. Andrié, A.M. Sprinkart, F.C. Schmeel, C. Stehning, R. Fimmers, J. Gieseke, C.P. Naehle, H.H. Schild, D.K. Thomas, Comprehensive cardiac magnetic resonance for short-term follow-up in acute myocarditis, J. Am. Heart Assoc. 5 (2016). doi:https://doi.org/10.1161/JAHA.116.003603

  85. 85.

    Anzini M, Merlo M, Sabbadini G, Barbati G, Finocchiaro G, Pinamonti B, Salvi A, Perkan A, Di Lenarda A, Bussani R, Bartunek J, Sinagra G (2013) Long-term evolution and prognostic stratification of biopsy-proven active myocarditis. Circulation. 128:2384–2394. https://doi.org/10.1161/CIRCULATIONAHA.113.003092

    Article  PubMed  Google Scholar 

  86. 86.

    Gräni C, Bière L, Eichhorn C, Kaneko K, Agarwal V, Aghayev A, Steigner M, Blankstein R, Jerosch-Herold M, Kwong RY (2019) Incremental value of extracellular volume assessment by cardiovascular magnetic resonance imaging in risk stratifying patients with suspected myocarditis. Int. J. Cardiovasc, Imaging. https://doi.org/10.1007/s10554-019-01552-6

    Google Scholar 

  87. 87.

    Moon JC, Messroghli DR, Kellman P, Piechnik SK, Robson MD, Ugander M, Gatehouse PD, Arai AE, Friedrich MG, Neubauer S, Schulz-Menger J, Schelbert EB (2013) Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson 15:92. https://doi.org/10.1186/1532-429X-15-92

    Article  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Aquaro GD, Ghebru Habtemicael Y, Camastra G, Monti L, Dellegrottaglie S, Moro C, Lanzillo C, Scatteia A, Di Roma M, Pontone G, Perazzolo Marra M, Barison A, Di Bella G (2019) Prognostic value of repeating cardiac magnetic resonance in patients with acute myocarditis. J Am Coll Cardiol 74:2439–2448. https://doi.org/10.1016/j.jacc.2019.08.1061

    Article  Google Scholar 

  89. 89.

    Birnie DH, Sauer WH, Bogun F, Cooper JM, Culver DA, Duvernoy CS, Judson MA, Kron J, Mehta D, Cosedis Nielsen J, Patel AR, Ohe T, Raatikainen P, Soejima K (2014) HRS expert consensus statement on the diagnosis and management of arrhythmias associated with cardiac sarcoidosis. Hear. Rhythm. 11:1304–1323. https://doi.org/10.1016/j.hrthm.2014.03.043

    Article  Google Scholar 

  90. 90.

    Olivotto I, Maron MS, Autore C, Lesser JR, Rega L, Casolo G, De Santis M, Quarta G, Nistri S, Cecchi F, Salton CJ, Udelson JE, Manning WJ, Maron BJ (2008) Assessment and significance of left ventricular mass by cardiovascular magnetic resonance in hypertrophic cardiomyopathy. J Am Coll Cardiol 52:559–566. https://doi.org/10.1016/j.jacc.2008.04.047

    Article  Google Scholar 

  91. 91.

    Webb J, Villa A, Bekri I, Shome J, Teall T, Claridge S, Jackson T, Porter B, Ismail TF, Di Giovine G, Rinaldi CA, Carr-White G, Al-Fakih K, Razavi R, Chiribiri A (2017) Usefulness of cardiac magnetic resonance imaging to measure left ventricular wall thickness for determining risk scores for sudden cardiac death in patients with hypertrophic cardiomyopathy. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2017.01.021

  92. 92.

    M.S. Maron, J.J. Finley, J.M. Bos, T.H. Hauser, W.J. Manning, T.S. Haas, J.R. Lesser, J.E. Udelson, M.J. Ackerman, B.J. Maron, Prevalence, clinical significance, and natural history of left ventricular apical aneurysms in hypertrophic cardiomyopathy, Circulation. (2008). doi:https://doi.org/10.1161/CIRCULATIONAHA.108.781401

  93. 93.

    X. Guo, C. Fan, L. Tian, Y. Liu, H. Wang, S. Zhao, F. Duan, X. Zhang, X. Zhao, F. Wang, H. Zhu, A. Lin, X. Wu, Y. Li, The clinical features, outcomes and genetic characteristics of hypertrophic cardiomyopathy patients with severe right ventricular hypertrophy, PLoS One. (2017). doi:https://doi.org/10.1371/journal.pone.0174118

  94. 94.

    Todiere G, Pisciella L, Barison A, Del Franco A, Zachara E, Piaggi P, Re F, Pingitore A, Emdin M, Lombardi M, Aquaro GD (2014) Abnormal T2-STIR magnetic resonance in hypertrophic cardiomyopathy: a marker of advanced disease and electrical myocardial instability. PLoS One 9:e111366. https://doi.org/10.1371/journal.pone.0111366

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Melacini P, Corbetti F, Calore C, Pescatore V, Smaniotto G, Pavei A, Bobbo F, Cacciavillani L, Iliceto S (2008) Cardiovascular magnetic resonance signs of ischemia in hypertrophic cardiomyopathy. Int J Cardiol 128:364–373. https://doi.org/10.1016/j.ijcard.2007.06.023

    Article  PubMed  Google Scholar 

  96. 96.

    Cecchi F, Olivotto I, Gistri R, Lorenzoni R, Chiriatti G, Camici PG (2003) Coronary microvascular dysfunction and prognosis in hypertrophic cardiomyopathy. N Engl J Med 349:1027–1035. https://doi.org/10.1056/NEJMoa025050

    CAS  Article  PubMed  Google Scholar 

  97. 97.

    O’Mahony C, Jichi F, Ommen SR, Christiaans I, Arbustini E, Garcia-Pavia P, Cecchi F, Olivotto I, Kitaoka H, Gotsman I, Carr-White G, Mogensen J, Antoniades L, Mohiddin SA, Maurer MS, Tang HC, Geske JB, Siontis KC, Mahmoud KD, Vermeer A, Wilde A, Favalli V, Guttmann OP, Gallego-Delgado M, Dominguez F, Tanini I, Kubo T, Keren A, Bueser T, Waters S, Issa IF, Malcolmson J, Burns T, Sekhri N, Hoeger CW, Omar RZ, Elliott PM (2018) International External Validation Study of the 2014 European Society of Cardiology guidelines on sudden cardiac death prevention in hypertrophic cardiomyopathy (EVIDENCE-HCM). Circulation 137:1015–1023. https://doi.org/10.1161/CIRCULATIONAHA.117.030437

    Article  PubMed  Google Scholar 

  98. 98.

    R.H. Chan, B.J. Maron, I. Olivotto, M.J. Pencina, G.E. Assenza, T. Haas, J.R. Lesser, C. Gruner, A.M. Crean, H. Rakowski, J.E. Udelson, E. Rowin, M. Lombardi, F. Cecchi, B. Tomberli, P. Spirito, F. Formisano, E. Biagini, C. Rapezzi, C.N. De Cecco, C. Autore, E.F. Cook, S.N. Hong, C.M. Gibson, W.J. Manning, E. Appelbaum, M.S. Maron, Prognostic value of quantitative contrast-enhanced cardiovascular magnetic resonance for the evaluation of sudden death risk in patients with hypertrophic cardiomyopathy, Circulation. 130 (2014) 484–495. doi:https://doi.org/10.1161/CIRCULATIONAHA.113.007094

  99. 99.

    Briasoulis A, Mallikethi-Reddy S, Palla M, Alesh I, Afonso L (2015) Myocardial fibrosis on cardiac magnetic resonance and cardiac outcomes in hypertrophic cardiomyopathy: a meta-analysis. Heart. 101:1406–1411. https://doi.org/10.1136/heartjnl-2015-307682

    CAS  Article  PubMed  Google Scholar 

  100. 100.

    Weng Z, Yao J, Chan RH, He J, Yang X, Zhou Y, He Y (2016) Prognostic value of LGE-CMR in HCM. JACC Cardiovasc Imaging 9:1392–1402. https://doi.org/10.1016/j.jcmg.2016.02.031

    Article  PubMed  Google Scholar 

  101. 101.

    Mentias A, Raeisi-Giglou P, Smedira NG, Feng K, Sato K, Wazni O, Kanj M, Flamm SD, Thamilarasan M, Popovic ZB, Lever HM, Desai MY (2018) Late gadolinium enhancement in patients with hypertrophic cardiomyopathy and preserved systolic function. J Am Coll Cardiol 72:857–870. https://doi.org/10.1016/j.jacc.2018.05.060

    Article  PubMed  Google Scholar 

  102. 102.

    Todiere G, Nugara C, Gentile G, Negri F, Bianco F, Falletta C, Novo G, Di Bella G, De Caterina R, Zachara E, Re F, Clemenza F, Sinagra G, Emdin M, Aquaro GD (2019) Prognostic role of late gadolinium enhancement in patients with hypertrophic cardiomyopathy and low-to-intermediate sudden cardiac death risk score. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2019.07.023

  103. 103.

    Kozor R, Nordin S, Treibel TA, Rosmini S, Castelletti S, Fontana M, Captur G, Baig S, Steeds RP, Hughes D, Manisty C, Grieve SM, Figtree GA, Moon JC (2017) Insight into hypertrophied hearts: a cardiovascular magnetic resonance study of papillary muscle mass and T1 mapping. Eur Hear J - Cardiovasc Imaging 18:1034–1040. https://doi.org/10.1093/ehjci/jew187

    Article  Google Scholar 

  104. 104.

    Chu LC, Corona-Villalobos CP, Halushka MK, Zhang Y, Pozzessere C, Kamel IR, Pozios I, Van Der Geest RJ, Gai N, Abraham RM, Abraham TP, Bluemke DA, Zimmerman SL (2017) Structural and functional correlates of myocardial T1 mapping in 321 patients with hypertrophic cardiomyopathy. J Comput Assist Tomogr 41:653–660. https://doi.org/10.1097/RCT.0000000000000564

    Article  PubMed  Google Scholar 

  105. 105.

    Kato S, Nakamori S, Bellm S, Jang J, Basha T, Maron M, Manning WJ, Nezafat R (2016) Myocardial native T1 time in patients with hypertrophic cardiomyopathy. Am J Cardiol 118:1057–1062. https://doi.org/10.1016/j.amjcard.2016.07.010

    Article  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Kramer CM, Appelbaum E, Desai MY, Desvigne-Nickens P, DiMarco JP, Friedrich MG, Geller N, Heckler S, Ho CY, Jerosch-Herold M, Ivey EA, Keleti J, Kim D-Y, Kolm P, Kwong RY, Maron MS, Schulz-Menger J, Piechnik S, Watkins H, Weintraub WS, Wu P, Neubauer S (2015) Hypertrophic cardiomyopathy registry: the rationale and design of an international, observational study of hypertrophic cardiomyopathy. Am Heart J 170:223–230. https://doi.org/10.1016/j.ahj.2015.05.013

    Article  PubMed  PubMed Central  Google Scholar 

  107. 107.

    D. Dalal, K. Nasir, C. Bomma, K. Prakasa, H. Tandri, J. Piccini, A. Roguin, C. Tichnell, C. James, S.D. Russell, D.P. Judge, T. Abraham, P.J. Spevak, D.A. Bluemke, H. Calkins, Arrhythmogenic right ventricular dysplasia: a United States experience, Circulation. (2005). doi:https://doi.org/10.1161/CIRCULATIONAHA.105.542266

  108. 108.

    S. Sen-Chowdhry, P. Syrris, D. Ward, A. Asimaki, E. Sevdalis, W.J. McKenna, Clinical and genetic characterization of families with arrhythmogenic right ventricular dysplasia/cardiomyopathy provides novel insights into patterns of disease expression, Circulation. (2007). doi:https://doi.org/10.1161/CIRCULATIONAHA.106.660241

  109. 109.

    F.I. Marcus, W.J. McKenna, D. Sherrill, C. Basso, B. Bauce, D.A. Bluemke, H. Calkins, D. Corrado, M.G.P.J. Cox, J.P. Daubert, G. Fontaine, K. Gear, R. Hauer, A. Nava, M.H. Picard, N. Protonotarios, J.E. Saffitz, D.M.Y. Sanborn, J.S. Steinberg, H. Tandri, G. Thiene, J.A. Towbin, A. Tsatsopoulou, T. Wichter, W. Zareba, Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: proposed modification of the Task Force Criteria., Eur. Heart J. 31 (2010) 806–814. doi:https://doi.org/10.1093/eurheartj/ehq025

  110. 110.

    Aquaro GD, Pingitore A, Di Bella G, Piaggi P, Gaeta R, Grigoratos C, Altinier A, Pantano A, Strata E, De Caterina R, Sinagra G, Emdin M (2018) Prognostic role of cardiac magnetic resonance in arrhythmogenic right ventricular cardiomyopathy. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2018.08.007

  111. 111.

    Jain A, Tandri H, Calkis H, Bluemke DA (2008) Role of cardiovascular magnetic resonance imaging in arrhythmogenic right ventricular dysplasia. J Cardiovasc Magn Reson. https://doi.org/10.1186/1532-429X-10-32

  112. 112.

    Nucifora G, Muser D, Masci PG, Barison A, Rebellato L, Piccoli G, Daleffe E, Toniolo M, Zanuttini D, Facchin D, Lombardi M, Proclemer A (2014) Prevalence and prognostic value of concealed structural abnormalities in patients with apparently idiopathic ventricular arrhythmias of left versus right ventricular origin: a magnetic resonance imaging study. Circ, Arrhythmia Electrophysiol. https://doi.org/10.1161/CIRCEP.113.001172

    Google Scholar 

  113. 113.

    Muser D, Santangeli P, Castro SA, Casado Arroyo R, Maeda S, Benhayon DA, Liuba I, Liang JJ, Sadek MM, Chahal A, Magnani S, Pieroni M, Santarossa E, Desjardins B, Dixit S, Garcia FC, Callans DJ, Frankel DS, Alavi A, Marchlinski FE, Selvanayagam JB, Nucifora G (2019) Risk stratification of patients with apparently idiopathic premature ventricular contractions. JACC Clin Electrophysiol 1040. https://doi.org/10.1016/j.jacep.2019.10.015

  114. 114.

    Aquaro GD, Barison A, Todiere G, Grigoratos C, Ait Ali L, Di Bella G, Emdin M, Festa P (2016) Usefulness of combined functional assessment by cardiac magnetic resonance and tissue characterization versus task force criteria for diagnosis of arrhythmogenic right ventricular cardiomyopathy. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2016.08.056

  115. 115.

    Negri F, De Luca A, Fabris E, Korcova R, Cernetti C, Grigoratos C, Aquaro GD, Nucifora G, Camici PG, Sinagra G (2019) Left ventricular noncompaction, morphological, and clinical features for an integrated diagnosis. Heart Fail Rev 24:315–323. https://doi.org/10.1007/s10741-018-9763-3

    Article  PubMed  Google Scholar 

  116. 116.

    Arbustini E, Favalli V, Narula N, Serio A, Grasso M (2016) Left ventricular noncompaction: a distinct genetic cardiomyopathy? J Am Coll Cardiol. https://doi.org/10.1016/j.jacc.2016.05.096

  117. 117.

    Captur G, Muthurangu V, Cook C, Flett AS, Wilson R, Barison A, Sado DM, Anderson S, McKenna WJ, Mohun TJ, Elliott PM, Moon JC (2013) Quantification of left ventricular trabeculae using fractal analysis. J Cardiovasc Magn Reson 15:36. https://doi.org/10.1186/1532-429X-15-36

    Article  PubMed  PubMed Central  Google Scholar 

  118. 118.

    Grothoff M, Pachowsky M, Hoffmann J, Posch M, Klaassen S, Lehmkuhl L, Gutberlet M (2012) Value of cardiovascular MR in diagnosing left ventricular non-compaction cardiomyopathy and in discriminating between other cardiomyopathies. Eur Radiol 22:2699–2709. https://doi.org/10.1007/s00330-012-2554-7

    Article  PubMed  PubMed Central  Google Scholar 

  119. 119.

    Jacquier A, Thuny F, Jop B, Giorgi R, Cohen F, Gaubert JY, Vidal V, Bartoli JM, Habib G, Moulin G (2010) Measurement of trabeculated left ventricular mass using cardiac magnetic resonance imaging in the diagnosis of left ventricular non-compaction. Eur Heart J 31:1098–1104. https://doi.org/10.1093/eurheartj/ehp595

    Article  PubMed  Google Scholar 

  120. 120.

    Petersen SE, Selvanayagam JB, Wiesmann F, Robson MD, Francis JM, Anderson RH, Watkins H, Neubauer S (2005) Left ventricular non-compaction. J Am Coll Cardiol 46:101–105. https://doi.org/10.1016/j.jacc.2005.03.045

    Article  PubMed  Google Scholar 

  121. 121.

    R.E. Hershberger, J. Lindenfeld, L. Mestroni, C.E. Seidman, M.R.G. Taylor, J.A. Towbin, Heart Failure Society of America, Genetic evaluation of cardiomyopathy--a Heart Failure Society of America practice guideline., J. Card. Fail. 15 (2009) 83–97. doi:https://doi.org/10.1016/j.cardfail.2009.01.006

  122. 122.

    Nucifora G, Aquaro GD, Pingitore A, Masci PG, Lombardi M (2011) Myocardial fibrosis in isolated left ventricular non-compaction and its relation to disease severity. Eur J Heart Fail 13:170–176. https://doi.org/10.1093/eurjhf/hfq222

    Article  PubMed  Google Scholar 

  123. 123.

    Mavrogeni S, Sfendouraki E, Theodorakis G, Kolovou G (2013) Diagnosis, severity grading and prognosis of left ventricular non-compaction using cardiovascular magnetic resonance. Int J Cardiol 167:598–599. https://doi.org/10.1016/j.ijcard.2012.09.234

    Article  PubMed  Google Scholar 

  124. 124.

    Ashrith G, Gupta D, Hanmer J, Weiss RM (2014) Cardiovascular magnetic resonance characterization of left ventricular non-compaction provides independent prognostic information in patients with incident heart failure or suspected cardiomyopathy. J Cardiovasc Magn Reson. https://doi.org/10.1186/s12968-014-0064-2

  125. 125.

    Andreini D, Pontone G, Bogaert J, Roghi A, Barison A, Schwitter J, Mushtaq S, Vovas G, Sormani P, Aquaro GD, Monney P, Segurini C, Guglielmo M, Conte E, Fusini L, Dello Russo A, Lombardi M, Gripari P, Baggiano A, Fiorentini C, Lombardi F, Bartorelli AL, Pepi M, Masci PG (2016) Long-term prognostic value of cardiac magnetic resonance in left ventricle noncompaction. J Am Coll Cardiol 68:2166–2181. https://doi.org/10.1016/j.jacc.2016.08.053

    Article  PubMed  Google Scholar 

  126. 126.

    A. Ivanov, D.S. Dabiesingh, G.P. Bhumireddy, A. Mohamed, A. Asfour, W.M. Briggs, J. Ho, S.A. Khan, A. Grossman, I. Klem, T.J. Sacchi, J.F. Heitner, Prevalence and prognostic significance of left ventricular noncompaction in patients referred for cardiac magnetic resonance imaging, Circ. Cardiovasc. Imaging. 10 (2017). doi:https://doi.org/10.1161/CIRCIMAGING.117.006174

  127. 127.

    Grigoratos C, Barison A, Ivanov A, Andreini D, Amzulescu M-S, Mazurkiewicz L, De Luca A, Grzybowski J, Masci PG, Marczak M, Heitner JF, Schwitter J, Gerber BL, Emdin M, Aquaro GD (2019) Meta-analysis of the prognostic role of late gadolinium enhancement and global systolic impairment in left ventricular noncompaction. JACC Cardiovasc Imaging 12:2141–2151. https://doi.org/10.1016/j.jcmg.2018.12.029

    Article  Google Scholar 

  128. 128.

    Zhou H, Lin X, Fang L, Zhao X, Ding H, Chen W, Xu R, Bai X, Wang Y, Fang Q (2016) Characterization of compacted myocardial abnormalities by cardiac magnetic resonance with native T1 mapping in left ventricular non-compaction patients: a comparison with late gadolinium enhancement. Circ J. https://doi.org/10.1253/circj.CJ-15-1269

  129. 129.

    Araujo-Filho JAB, Assuncao AN, Tavares de Melo MD, Bière L, Lima CR, Dantas RN, Nomura CH, Salemi VMC, Jerosch-Herold M, Parga JR (2018) Myocardial T1 mapping and extracellular volume quantification in patients with left ventricular non-compaction cardiomyopathy. Eur. Hear. J. - Cardiovasc. Imaging. 19:888–895. https://doi.org/10.1093/ehjci/jey022

    Article  Google Scholar 

  130. 130.

    Merlo M, Gobbo M, Stolfo D, Losurdo P, Ramani F, Barbati G, Pivetta A, Di Lenarda A, Anzini M, Gigli M, Pinamonti B, Sinagra G (2016) The prognostic impact of the evolution of RV function in idiopathic DCM. JACC Cardiovasc Imaging 9:1034–1042. https://doi.org/10.1016/j.jcmg.2016.01.027

    Article  PubMed  Google Scholar 

  131. 131.

    Merlo M, Stolfo D, Gobbo M, Gabassi G, Barbati G, Naso P, Secoli G, Boscutti A, Ramani F, Gigli M, Pinamonti B, Sinagra G (2019) Prognostic impact of short-term changes of E/E’ ratio and left atrial size in dilated cardiomyopathy. Eur J Heart Fail 21:1294–1296. https://doi.org/10.1002/ejhf.1543

    Article  PubMed  Google Scholar 

  132. 132.

    Stolfo D, De Luca A, Morea G, Merlo M, Vitrella G, Caiffa T, Barbati G, Rakar S, Korcova R, Perkan A, Pinamonti B, Pappalardo A, Berardini A, Biagini E, Saia F, Grigioni F, Rapezzi C, Sinagra G (2018) Predicting device failure after percutaneous repair of functional mitral regurgitation in advanced heart failure: implications for patient selection. Int J Cardiol 257:182–187. https://doi.org/10.1016/j.ijcard.2018.01.009

    Article  PubMed  Google Scholar 

  133. 133.

    A. Porcari, M. Merlo, L. Crosera, D. Stolfo, G. Barbati, F. Biondi, G. De Angelis, A. Paldino, L. Pagnan, M. Belgrano, M.A. Cova, B. Pinamonti, G. Vitrella, G. Sinagra, Strain analysis reveals subtle systolic dysfunction in confirmed and suspected myocarditis with normal LVEF. A cardiac magnetic resonance study, Clin. Res. Cardiol. (2019). doi:https://doi.org/10.1007/s00392-019-01577-w

  134. 134.

    A. Cannatà, G. De Angelis, A. Boscutti, C. Normand, J. Artico, P. Gentile, M. Zecchin, S. Heymans, M. Merlo, G. Sinagra, Arrhythmic risk stratification in non-ischaemic dilated cardiomyopathy beyond ejection fraction, Heart. (2020). doi:https://doi.org/10.1136/heartjnl-2019-315942

  135. 135.

    Zeidan-Shwiri T, Yang Y, Lashevsky I, Kadmon E, Kagal D, Dick A, Laish Farkash A, Paul G, Gao D, Shurrab M, Newman D, Wright G, Crystal E (2015) Magnetic resonance estimates of the extent and heterogeneity of scar tissue in ICD patients with ischemic cardiomyopathy predict ventricular arrhythmia. Hear. Rhythm. 12:802–808. https://doi.org/10.1016/j.hrthm.2015.01.007

    Article  Google Scholar 

  136. 136.

    Alexandre J, Saloux E, Dugué AE, Lebon A, Lemaitre A, Roule V, Labombarda F, Provost N, Gomes S, Scanu P, Milliez P (2013) Scar extent evaluated by late gadolinium enhancement CMR: a powerful predictor of long term appropriate ICD therapy in patients with coronary artery disease. J Cardiovasc Magn Reson 15:12. https://doi.org/10.1186/1532-429X-15-12

    Article  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Krittayaphong R, Saiviroonporn P, Boonyasirinant T, Udompunturak S (2011) Prevalence and prognosis of myocardial scar in patients with known or suspected coronary artery disease and normal wall motion. J Cardiovasc Magn Reson 13:2. https://doi.org/10.1186/1532-429X-13-2

    Article  PubMed  PubMed Central  Google Scholar 

  138. 138.

    Scott PA, Morgan JM, Carroll N, Murday DC, Roberts PR, Peebles CR, Harden SP, Curzen NP (2011) The extent of left ventricular scar quantified by late gadolinium enhancement MRI is associated with spontaneous ventricular arrhythmias in patients with coronary artery disease and implantable cardioverter-defibrillators. Circ Arrhythmia Electrophysiol 4:324–330. https://doi.org/10.1161/CIRCEP.110.959544

    Article  Google Scholar 

  139. 139.

    Kwon DH, Halley CM, Carrigan TP, Zysek V, Popovic ZB, Setser R, Schoenhagen P, Starling RC, Flamm SD, Desai MY (2009) Extent of left ventricular scar predicts outcomes in ischemic cardiomyopathy patients with significantly reduced systolic function. JACC Cardiovasc Imaging 2:34–44. https://doi.org/10.1016/j.jcmg.2008.09.010

    Article  PubMed  Google Scholar 

  140. 140.

    Piers SRD, Everaerts K, van der Geest RJ, Hazebroek MR, Siebelink H-M, Pison LAFG, Schalij MJ, Bekkers SCAM, Heymans S, Zeppenfeld K (2015) Myocardial scar predicts monomorphic ventricular tachycardia but not polymorphic ventricular tachycardia or ventricular fibrillation in nonischemic dilated cardiomyopathy. Hear Rhythm 12:2106–2114. https://doi.org/10.1016/j.hrthm.2015.05.026

    Article  Google Scholar 

  141. 141.

    Masci PG, Doulaptsis C, Bertella E, Del Torto A, Symons R, Pontone G, Barison A, Droogné W, Andreini D, Lorenzoni V, Gripari P, Mushtaq S, Emdin M, Bogaert J, Lombardi M (2014) Incremental prognostic value of myocardial fibrosis in patients with non-ischemic cardiomyopathy without congestive heart failure. Circ Hear Fail 7:448–456. https://doi.org/10.1161/CIRCHEARTFAILURE.113.000996

    Article  Google Scholar 

  142. 142.

    Assomull RG, Prasad SK, Lyne J, Smith G, Burman ED, Khan M, Sheppard MN, Poole-Wilson PA, Pennell DJ (2006) Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J Am Coll Cardiol 48:1977–1985. https://doi.org/10.1016/j.jacc.2006.07.049

    Article  PubMed  Google Scholar 

  143. 143.

    Imazio M, Angelico G, Andriani M, Lobetti-Bodoni L, Davini O, Giustetto C, Rinaldi M (2018) Prevalence and prognostic impact of septal late gadolinium enhancement in acute myocarditis with or without preserved left ventricular function. Am J Cardiol 122:1955–1958. https://doi.org/10.1016/j.amjcard.2018.08.038

    Article  PubMed  Google Scholar 

  144. 144.

    Maron MS, Appelbaum E, Harrigan CJ, Buros J, Gibson CM, Hanna C, Lesser JR, Udelson JE, Manning WJ, Maron BJ (2008) Clinical profile and significance of delayed enhancement in hypertrophic cardiomyopathy. Circ. Hear. Fail. 1:184–191. https://doi.org/10.1161/CIRCHEARTFAILURE.108.768119

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marco Merlo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Porcari, A., De Luca, A., Grigoratos, C. et al. Arrhythmic risk stratification by cardiac magnetic resonance tissue characterization: disclosing the arrhythmic substrate within the heart muscle. Heart Fail Rev (2020). https://doi.org/10.1007/s10741-020-09986-0

Download citation

Keywords

  • Sudden cardiac death
  • Arrhythmic stratification
  • Cardiac magnetic resonance
  • Late gadolinium enhancement
  • Mapping imaging
  • Cardiomyopathies