The International Journal of Cardiovascular Imaging

, Volume 35, Issue 12, pp 2221–2229 | Cite as

Diagnostic and prognostic value of cardiac magnetic resonance in acute myocarditis: a systematic review and meta-analysis

  • Sarah Blissett
  • Yehuda Chocron
  • Bojan Kovacina
  • Jonathan AfilaloEmail author
Original Paper


While diagnostic criteria were elaborated for acute myocarditis using cardiac magnetic resonance (CMR) in 2009, studies have since examined the yield of traditional and novel CMR parameters to achieve greater accuracy and to predict clinical outcomes. The purpose of this systematic review and meta-analysis was to determine the diagnostic and prognostic value of CMR parameters for acute myocarditis. MEDLINE and EMBASE were systematically searched for original studies that reported CMR parameters in adult patients suspected of acute myocarditis. Each CMR parameter's binary prevalence, mean value and standard deviation were extracted. Parameters were meta-analyzed using a random-effects model to generate standardized mean differences. After screening 1492 abstracts, 53 studies were included encompassing 2823 myocarditis patients and 803 controls. Pooled standardized mean differences between myocarditis patients and controls were: T2 mapping time 2.26 (95% CI 1.50–3.02), extracellular volume 1.64 (95% CI 0.87–2.42), LGE percentage 1.30 (95% CI 0.95–1.64), T1 mapping time 1.18 (95% CI 0.35–2.01), T2 ratio 1.17 (95% CI 0.80–1.54), and EGE ratio 0.93 (95% CI 0.66–1.19). Prolonged T1 mapping time had the highest sensitivity (82%), pericardial effusion had the highest specificity (99%). Baseline LV dysfunction and the presence of LGE were predictive of major adverse cardiac events. The results support integration of parametric mapping criteria in the diagnostic criteria for myocarditis. The presence of baseline LV dysfunction and LGE predict patients at higher risk of adverse events.


Acute myocarditis Cardiac magnetic resonance Lake Louise criteria Parametric mapping Meta-analysis 



Sarah Blissett is grateful for support from the Western University Resident Research Career Development Funding.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10554_2019_1674_MOESM1_ESM.docx (1.4 mb)
Supplementary file1 (DOCX 1407 kb)


  1. 1.
    Assomull RG, Lyne JC, Keenan N, Gulati A, Bunce NH, Davies SW, Pennel DJ, Prasad SK (2007) The role of cardiovascular magnetic resonance in patients presenting with chest pain, raised troponin, and unobstructed coronary arteries. Eur Heart J 28:1242–1249PubMedGoogle Scholar
  2. 2.
    Doolan A, Langlois N, Semsarian C (2004) Causes of sudden cardiac death in young Australians. Med J Aust 180:110–112PubMedGoogle Scholar
  3. 3.
    Felker GM, Thompson RE, Hare JM, Hruban RH, Clemetson DE, Howard DL, Haughman KL, Kasper EK (2003) Underlying causes and long-term survival in patients with initially unexplained cardiomyopathy. N Engl J Med 342:1077–1084Google Scholar
  4. 4.
    Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, White JA, Abdel-Aty H, Gutberlet M, Prasad S, Aletras A (2009) Cardiovascular magnetic resonance in myocarditis: a JACC White Paper. J Am Coll Cardiol 53:1475–1487PubMedPubMedCentralGoogle Scholar
  5. 5.
    Messroghli DR, Moon JC, Ferreira VM, Grosse-Wortmann L, He T, Kellman P, Mascherbauer J, Nezafat R, Salerno M, Schelbert EB, Taylor AJ (2017) 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 19:75PubMedPubMedCentralGoogle Scholar
  6. 6.
    Ferreira VM, Piechnik SK, Dall’Armellina E, Karamitsos TD, Francis JM, Ntusi N, Holloway C, Choudhury RP, Kardos A, Robson MD, Friedrich MG, (2013) T1 mapping for the diagnosis of acute myocarditis using CMR: comparison to T2-weighted and late gadolinium enhanced imaging. JACC Cardiovasc Imaging 6:1048–1058PubMedGoogle Scholar
  7. 7.
    Bohnen S, Radunski UK, Lund GK, Kandolf R, Stehning C, Schnackenburg B, Gerhard A, Blankenberg, Muellerleile K (2015) Performance of T1 and T2 mapping cardiovascular magnetic resonance to detect active myocarditis in patients with recent-onset heart failure. Circ Cardiovasc Imaging 8:6. CrossRefGoogle Scholar
  8. 8.
    Radunski UK, Lund GK, Stehning C, Schnackenburg B, Bohnen S, Gerdhard A, Blankenberg, Muellerleile K (2014) CMR in patients with severe myocarditis: diagnostic value of quantitative tissue markers including extracellular volume imaging JACC Cardiovasc Imaging 7:667–675PubMedGoogle Scholar
  9. 9.
    Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350:7647Google Scholar
  10. 10.
    Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A (2016) Rayyan-a web and mobile app for systematic reviews. Syst Rev 5:210PubMedPubMedCentralGoogle Scholar
  11. 11.
    Wells G, Shea B, O’Connell D, Peterson J, Welch, V, Losos M, Tugwell P (2014) Newcastle–Ottawa quality assessment scale cohort studies. Accessed 31 Jul 2017
  12. 12.
    Faraone SV (2008) Interpreting estimates of treatment effects: implications for managed care. J Clin Pharm Ther 33:700–711Google Scholar
  13. 13.
    Abdel-Aty H, Boye P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich M, Schulz-Menger J (2005) Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol. PubMedGoogle Scholar
  14. 14.
    Ammirati E, Moroni F, Sormani P, Peritore A, Milazzo A, Quattrocchi G, Cipriani M, Oliva F, Giannattasio C, Frigerio M, Roghi A (2017) Quantitative changes in late gadolinium enhancement at cardiac magnetic resonance in the early phase of acute myocarditis. Int J Cardiol 231:216–221PubMedGoogle Scholar
  15. 15.
    Andre F, Stock FT, Riffel J, Giannitsis E, Steen H, Scharhag J, Katus HA, Buss SJ (2016) Incremental value of cardiac deformation analysis in acute myocarditis: a cardiovascular magnetic resonance imaging study. Int J Cardiovasc Imaging 32:1093–1101PubMedGoogle Scholar
  16. 16.
    Baebler B, Schaarschmidt F, Dick A, Stehning C, Schnackenburg B, Michels G, Maintz D, Bunck AC (2015) Mapping tissue inhomogeneity in acute myocarditis: a novel analytical approach to quantitative myocardial edema imaging by T2-mapping. J Cardiovasc Magn Reson. CrossRefGoogle Scholar
  17. 17.
    Barone-Rochette G, Augier C, Rodiere M, Quesada JL, Foote A, Bouvaist H, Marliere Fagret D, Baguet JP, Vanzetto G (2014) Potentially simple score of late gadolinium enhancement cardiac MR in acute myocarditis outcome. J Magn Reson Imaging 40:1347–1354PubMedGoogle Scholar
  18. 18.
    Camastra GS, Cacciotti L, Marconi F, Sbarbati S, Pironi B, Ansalone G (2007) Late enhancement detected by cardiac magnetic resonance imaging in acute myocarditis mimicking acute myocardial infarction: location patterns and lack of correlation with systolic function. J Cardiovasc Med 8:1029–1033Google Scholar
  19. 19.
    Chopra H, Arangalage D, Bouleti C, Zarka S, Fayard F, Chillon S, Laissy JP, Henry-Feugeas MC, Steg PG, Vahanian A, Ou P (2016) Prognostic value of the infarct- and non-infarct like patterns and cardiovascular magnetic resonance parameters on long-term outcome of patients after acute myocarditis. Int J Cardiol 212:63–69PubMedGoogle Scholar
  20. 20.
    Chu G, Flewitt J, Mikami Y, Vermes E, Friedrich M (2013) Assessment of acute myocarditis by cardiovascular MR: diagnostic performance of shortened protocols. Int J Cardiovasc Imaging 29:1077–1083PubMedGoogle Scholar
  21. 21.
    Cocker MS, Abdel-Aty H, Strohm O, Friedrich MG (2009) Age and gender effects on the extent of myocardial involvement in acute myocarditis: a cardiovascular magnetic resonance study. Heart 95:1925–1930PubMedGoogle Scholar
  22. 22.
    Danti M, Sbarbati S, Alsadi N, Di Filippo A, Gangitano G, Giglio L, Salvini V, Amoruso M, Camastra GS, Ansalone G, Della Sala S (2009) Cardiac magnetic resonance imaging: diagnostic value and utility in the follow-up of patients with acute myocarditis mimicking myocardial infarction. Radiol Med 114:229–238PubMedGoogle Scholar
  23. 23.
    De Lazzari M, Zorzi A, Baritussio A, Siciliano M, Migliore F, Susana A, Giorgi B, Lacognata C, Iliceto S, Marra MP, Corrado D (2016) Relationship between T-wave inversion and transmural myocardial edema as evidenced by cardiac magnetic resonance in patients with clinically suspected acute myocarditis: clinical and prognostic implications. J Electrocardiol 49:587–595PubMedGoogle Scholar
  24. 24.
    Deux J-F, Maatouk M, Lim P, Vignaud A, Mayer J, Gueret P, Rahmouni A (2011) Acute myocarditis: diagnostic value of contrast-enhanced cine steady-state free precession MRI sequences. AJR 197:1081–1087PubMedGoogle Scholar
  25. 25.
    Florian A, Schaufele T, Ludwig A, Rosch S, Wenzelburger I, Yildiz H, Sechtem U, Yilmaz A (2015) Diagnostic value of CMR in young patients with clinically suspected acute myocarditis is determined by cardiac enzymes. Clin Res Cardiol 104:154–163PubMedGoogle Scholar
  26. 26.
    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 7:254–263PubMedGoogle Scholar
  27. 27.
    Gahide G, Bertrand D, Roubille F, Tron C, Skaik S, Piot C, Leclerq F, Cribier A, Vernhet H, Dacher JN (2010) MR delayed enhancement imaging findings in suspected acute myocarditis. Eur Radiol 20:65–72PubMedGoogle Scholar
  28. 28.
    Goitein O, Matetzky S, Beinart R, Di Segni E, Hod H, Bentancur A, Konen E (2009) Acute myocarditis: noninvasive evaluation with cardiac MRI and transthoracic echocardiography. AJR 192:254–258PubMedGoogle Scholar
  29. 29.
    Grun S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, Kispert EM, Hill S, Ong P, Klingel K, Kandolf R (2012) Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery. J Am Coll Cardiol 59:1604–1615PubMedGoogle Scholar
  30. 30.
    Hinojar R, Foote L, Arroyo Ucar E, Jackson T, Jabbour A, Yu CY, McCrohon J, Higgins DM, Carr-White G, Mayr M, Nagel E (2015) Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis: a proposed diagnostic algorithm using CMR. JACC Cardiovasc Imaging 8:37–46PubMedGoogle Scholar
  31. 31.
    Ingkanisorn WP, Paterson DI, Calvo KR, Rosing DR, Schwartzentruber DJ, Fuisz AR, Arai AE (2006) Cardiac magnetic resonance appearance of myocarditis caused by high dose IL-2: similarities to community-acquired myocarditis. J Cardiovasc Magn Reson 8:353–360PubMedGoogle Scholar
  32. 32.
    Jeserich M, Olschewski M, Bley T, Merkle N, Kirchberger J, Pavlik G, Bode C, Geibel A (2009) Cardiac involvement after respiratory tract viral infection-detection by cardiac magnetic resonance. J Comput Assist Tomogr 33:15–19PubMedGoogle Scholar
  33. 33.
    Jeserich M, Olschewski M, Kimmel S, Bode C, Geibel A (2014) Acute results and long-term follow-up of patients with accompanying myocarditis after viral respiratory or gastrointestinal tract infection. Int J Cardiol 174:853–855PubMedGoogle Scholar
  34. 34.
    Laissy J-P, Messin B, Varenne O, Iung B, Karila-Cohen D, Schouman-Claeys E, Steg PG (2002) MRI of acute myocarditis. Chest 122:1638–1648PubMedGoogle Scholar
  35. 35.
    Luetkens JA, Homsi R, Dabir D, Kuetting DL, Marx C, Doerner J, Schlesinger-Irsch U, Andrie R, Sprinkart AM, Schmeel FC, Stehning C (2016) Comprehensive cardiac magnetic resonance for short-term follow-up in acute myocarditis. J Am Heart Assoc. CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Lurz P, Eitel I, Adam J, Steiner J, Grothoff M, Desch S, Fuernau G, De Waha S, Sareban M, Leucke C, Klingel K (2012) Diagnostic performance of CMR imaging compared with EMB in patients with suspected myocarditis. JACC Cardiovasc Imaging 5:513–524PubMedGoogle Scholar
  37. 37.
    Lurz P, Luecke C, Eitel I, Fohrenbach F, Frank C, Grothoff M, de Waha S, Rommel KP, Lurz JA, Klingel K, Kandolf R (2016) Comprehensive cardiac magnetic resonance imaging in patients with suspected myocarditis: the MyoRacer-trial. J Am Coll Cardiol 67:1800–1811PubMedGoogle Scholar
  38. 38.
    Mahrholdt H, Wagner A, Deluigi CC, Kispert E, Hager S, Meinhardt G, Vogelsberg H (2006) Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 114:1581–1590PubMedGoogle Scholar
  39. 39.
    Mavrogeni S, Spargias C, Bratis C, Kolovou G, Markussis V, Papadopoulou E, Constadoulakis P, Papadimitropoulos M, Douskou M, Pavlides G, Cokkinos D (2011) Myocarditis as a precipitating factor for heart failure: evaluation and 1-year follow-up using cardiovascular magnetic resonance and endomyocardial biopsy. Eur J Heart Fail 13:830–837PubMedGoogle Scholar
  40. 40.
    Melendez-Ramirez G, de Micheli A, Soto ME, Meave-Gonzalez A, Kimura-Hayama E, Alcantara M, Gonzalez-Pacheco H (2014) Agreement between ST elevation and late enhancement evaluated by MRI in patients with acute myocarditis. J Electrocardiol 47:212–218PubMedGoogle Scholar
  41. 41.
    Mewton N, Dernis A, Bresson D, Zouaghi O, Croisille P, Flocard E, Douek P, Bonnefoy-Cudraz E (2015) Myocardial biomarkers and delayed enhanced cardiac magnetic resonance relationship in clinically suspected myocarditis and insight on clinical outcome. J Cardiovasc Med 16:696–703Google Scholar
  42. 42.
    Natale L, De Vita A, Baldari C, Meduri A, Pieroni M, Lombardo A, Crea F, Bonomo L (2012) Correlation between clinical presentation and delayed-enhancement MRI pattern in myocarditis. Radiol med 117:1309–1319PubMedGoogle Scholar
  43. 43.
    Ong P, Athansiadis A, Hill S, Kispert EM, Borgulya G, Klingel K, Kandolf R, Sechtem U, Mahrholdt H (2011) Usefulness of pericardial effusion as new diagnostic criterion for noninvasive detection of myocarditis. Am J Cardiol 108:445–452PubMedGoogle Scholar
  44. 44.
    Perfetti M, Malatesta G, Alvarez I, Liga R, Barison A, Todiere G, Eletto N, De Caterine R, Lombardi M, Aquaro GD (2014) A fast and effective method to assess myocardial hyperemia in acute myocarditis by magnetic resonance. Int J Cardiovasc Imaging 30:629–637PubMedGoogle Scholar
  45. 45.
    Puntmann VO, Taylor PC, Barr A, Schnackenburg B, Jahnke C, Paetsch I (2010) Towards understanding the phenotypes of myocardial involvement in the presence of self-limiting and sustained systemic inflammation: a magnetic resonance imaging study. Rheumatology 49:528–535PubMedGoogle Scholar
  46. 46.
    Radunski U, Lund G, Saring D, Bohnen S, Stehning C, Schnackenburg B, Avanesov M, Tahir E, Adam G, Blankenberg S, Muellerleile K (2017) T1 and T2 mapping cardiovascular magnetic resonance imaging techniques reveal unapparent myocardial injury in patients with myocarditis. Clin Res Cardiol. CrossRefPubMedGoogle Scholar
  47. 47.
    Rottgen R, Christiani R, Freyhardt P, Gutberlet M, Schultheiss HP, Hamm B, Kuhl U (2011) Magnetic resonance imaging findings in acute myocarditis and correlation with immunohistological parameters. Eur Radiol 21:1259–1266PubMedGoogle Scholar
  48. 48.
    Sanguineti F, Garot P, Mana M, O’h-Ici D, Hovasse T, Unterseeh T, Louvard Y, Troussier X, Morice MC, Garot J (2015) Cardiovascular magnetic resonance predictors of clinical outcome in patients with suspected acute myocarditis. J Cardiovasc Magn Reson 17:78.Google Scholar
  49. 49.
    Schumm J, Greulich S, Wagner A, Grun S, Ong P, Bentz K, Klingel K, Kandolf R, Bruder O, Schneider S, Sechtem U (2014) Cardiovascular magnetic resonance risk stratification in patients with clinically suspected myocarditis. J Cardiovasc Magn Reson 16:14PubMedPubMedCentralGoogle Scholar
  50. 50.
    Schwab J, Rogg HJ, Pauschinger M, Fessele K, Bareiter T, Bär I, Loose R (2016) Functional and morphological parameters with tissue characterization of cardiovascular magnetic imaging in clinically verified “infarct-like myocarditis. RöFo Fortschr Geb Röntgenstrahlen bildgeb Verfahr 188:365–373Google Scholar
  51. 51.
    Spieker M, Haberkorn S, Gastl M, Behm P, Katsianos S, Horn P, Jacoby C, Schnackenburg B, Reinecke P, Kelm M, Westenfeld R (2017) Abnormal T2 mapping cardiovascular magnetic resonance correlates with adverse clinical outcome in patients with suspected acute myocarditis. J Cardiovasc Magn Reson 19:38PubMedPubMedCentralGoogle Scholar
  52. 52.
    Šramko M, Kubánek M, Tintěra J, Kautznerová D, Weichet J, Malušková J, Franekova J, Kautzner J (2013) Utility of combination of cardiac magnetic resonance imaging and high-sensitivity cardiac troponin T assay in diagnosis of inflammatory cardiomyopathy. Am J Cardiol 111:258–264PubMedGoogle Scholar
  53. 53.
    Stensaeth KH, Hoffmann P, Fossum E, Mangschau A, Sandvik L, Klow NE (2012) Cardiac magnetic resonance visualizes acute and chronic myocardial injuries in myocarditis. Int J Cardiovasc Imaging 28:327–335PubMedGoogle Scholar
  54. 54.
    Thavendiranathan P, Walls M, Giri S, Verhaert D, Rajagopalan S, Moore S, Simonetti OP, Raman SV (2012) Improved detection of myocardial involvement in acute inflammatory cardiomyopathies using T2 mapping. Circ Cardiovasc Imaging 5:102–110PubMedGoogle Scholar
  55. 55.
    Toussaint M, Gilles RJ, Azzabou N, Marty B, Vignaud A, Greiser A, Carlier PG (2015) Characterization of benign myocarditis using quantitative delayed-enhancement imaging based on Molli T1 mapping. Medicine 94:e1868PubMedPubMedCentralGoogle Scholar
  56. 56.
    Vermes E, Childs H, Faris P, Friedrich MG (2014) Predictive value of CMR criteria for LV functional improvement in patients with acute myocarditis. Eur Heart J Cardiovasc Imaging 15:1140–1144PubMedGoogle Scholar
  57. 57.
    Von Knobelsdorff-Brenkenhoff F, Schuler MJ, Doganguzel MS, Dieringer MMA, Rudolph PA, Greiser MA, Kellman P, Schulz-Menger J (2017) Detection and monitoring of acute myocarditis applying quantitative cardiovascular magnetic resonance. Circ Cardiovasc Imaging.
  58. 58.
    Wagner A, Schulz-Menger J, Dietz R, Friedrich MG (2003) Long-term follow-up of patients with acute myocarditis by magnetic resonance imaging. MAGMA 16:17–20PubMedGoogle Scholar
  59. 59.
    Weigand J, Nielsen JC, Sengupta PP, Sanz J, Srivastava S, Uppu S (2016) Feature tracking-derived peak systolic strain compared to late gadolinium enhancement in troponin-positive myocarditis: a case–control study. Pediatr Cardiol 37:696–703PubMedGoogle Scholar
  60. 60.
    Yelgec N, Dymarkowski S, Ganame J, Bogaert J (2007) Value of MRI in patients with a clinical suspicion of acute myocarditis. Eur Radiol 17:2211–2217PubMedGoogle Scholar
  61. 61.
    Zagrosek A, Abdel-Aty H, Boye P, Wassmuth R, Messroghli D, Utz W, Rudolph A, Bohl S, Dietz R, Schulz-Menger J (2009) Cardiac magnetic resonance monitors reversible and irreversible myocardial injury in myocarditis. JACC Cardiovasc Imaging 2:131–138PubMedGoogle Scholar
  62. 62.
    Zarka S, Bouleti C, Arangalage D, Chopra H, Chillon S, Henry-Feugeas MC, Abtan J, Juliard JM, Iung B, Vahanian A, Laissy JP (2016) Usefulness of subepicardial hyperemia on contrast-enhanced first-pass magnetic resonance perfusion imaging for diagnosis of acute myocarditis. Am J Cardiol 118:440–445PubMedGoogle Scholar
  63. 63.
    Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U, Kindermann I, Gutberlet M, Cooper LT, Liu P, Friedrich MG (2018) Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations. J Am Coll Cardiol 24:3158–3176Google Scholar
  64. 64.
    Kotanidis CP, Bazmpani MA, Haidich AB, Karvounis C, Antoniades C, Karamitsos TD (2018) Diagnostic accuracy of cardiovascular magnetic resonance in acute myocarditis: a systematic review and meta-analysis. JACC Cardiovasc Imaging 17:31182–31188Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sarah Blissett
    • 1
  • Yehuda Chocron
    • 2
  • Bojan Kovacina
    • 3
  • Jonathan Afilalo
    • 1
    • 2
    • 4
    Email author
  1. 1.Division of Cardiology, Azrieli Heart Centre, Jewish General HospitalMcGill UniversityMontrealCanada
  2. 2.Centre for Clinical Epidemiology, Lady Davis Institute for Medical Research, Jewish General HospitalMcGill UniversityMontrealCanada
  3. 3.Department of Radiology, Jewish General HospitalMcGill UniversityMontrealCanada
  4. 4.McGill Integrated Cardiac Imaging Fellowship ProgramJewish General HospitalMontrealCanada

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