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Acute myocarditis with autoimmune features: one-year follow-up with CMR

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Abstract

In this prospective study on patients with acute myocarditis (AM), we aimed to describe the new concept of AMAF (AM with autoimmune features) similar to the previously described interstitial pneumonia with autoimmune features (IPAF). IPAF has recently emerged as a new entity, and IPAF patients appear to have fewer episodes of exacerbation and better survival than patients with idiopathic pulmonary fibrosis. Consecutive patients with infarct-like CMR-confirmed AM were classified AMAF if their serologic status measured from blood sampled at presentation was positive (antinuclear antibodies (ANA) ≥ 1:320), but without meeting established classification criteria for connective tissue disease (CTD). The myocardial tissue abnormalities and their progression were assessed on cardiac magnetic resonance (CMR) within 7 days following symptom onset and at 1 year according to their seropositivity. Among the 64 AM patients included, seven presented AMAF (11%). At baseline CMR, patients with AMAF had half as much late gadolinium enhancement (LGE) as seronegative AM patients (4.41% (1.47–4.41) of myocardial volume versus 8.82% (5.88–14.71), p = 0.01, respectively). At 1-year of follow-up, persistent myocardial scarring was less frequent in AMAF patients (n = 2 (28.6%) than seronegative AM patients (n = 38 (66.7%) (p = 0.021). AMAF, diagnosed as seropositive AM without a specific autoimmune disease, is not rare and is associated with less extensive LGE in the acute phase. In addition, AMAF patients had more favorable outcomes on 12-month CMR. Prospective studies are needed to address the clinical significance of this new concept and its long-term cardiovascular impact.

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References

  1. Caforio ALP, Marcolongo R, Basso C, Iliceto S (2015) Clinical presentation and diagnosis of myocarditis. Heart 101:1332–1344

    Article  CAS  Google Scholar 

  2. Cooper LT (2009) Myocarditis. N Engl J Med 360:1526–1538

    Article  CAS  Google Scholar 

  3. Caforio AL, Pankuweit S, Arbustini S, Basso C, Gimeno-Blanes J, Felix SB, Fu M, Helio T, Heymans S, Jahns R, Klingel K, Linhart A, Maisch B, McKenna W, Mogensen J, Pinto YM, Ristic A, Schultheiss HP, Seggewiss H, Tavazzi L, Thiene G, Yilmaz A, Charron A, Elliott PM (2013) European Society of Cardiology Working Group on Myocardial and Pericardial Diseases, 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 34:2636–2648

    Article  Google Scholar 

  4. Mahrholdt H, Wagner A, Deluigi CC, Kispert E, Hager S, Meinhardt G, Vogelsberg H, Fitz P, Dippon J, Bock C-T, Kingel K, Kandolf R, Sechtem U (2006) Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 114:1581–2190

    Article  Google Scholar 

  5. Eckart RE, Scoville SL, Campbell CL, Shru EA, Stajduhar KC, Potter RN, Pearse LA, Virmani R (2004) Sudden death in young adults: a 25-year review of autopsies in military recruits. Ann Intern Med 141:829–834

    Article  Google Scholar 

  6. Kasper EK, Agema WR, Hutchins GM, Deckers JW, Hare JM, Baughman KL (1994) The causes of dilated cardiomyopathy: a clinicopathologic review of 673 consecutive patients. J Am Coll Cardiol 23:586–590

    Article  CAS  Google Scholar 

  7. Gräni C, Eichhorn C, Bière L, 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 70:1964–1976

    Article  Google Scholar 

  8. 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) “Cardiac Magnetic Resonance” Working Group of the Italian Society of Cardiology, Prognostic value of repeating cardiac magnetic resonance in patients with acute myocarditis. J Am Coll Cardiol 74:2439–2448

    Article  Google Scholar 

  9. Sambataro G, Sambataro D, Torrisi SS, Vancheri A, Pavone M, Rosso R, Schisano M, Crimi C, Pignataro F, Fischer A, Del Papa N, Vancheri C (2018) State of the art in interstitial pneumonia with autoimmune features: a systematic review on retrospective studies and suggestions for further advances. Eur Respir Rev 27:170139

    Article  Google Scholar 

  10. Lee CT, Oldham JM (2017) Interstitial pneumonia with autoimmune features: overview of proposed criteria and recent cohort characterization. Clin Pulm Med 24:191–196

    Article  Google Scholar 

  11. Oldham JM, Adegunsoye A, Valenzi E, Lee C, Witt L, Chen L, Husain AN, Montner S, Chung JH, Cottin V, Fischer A, Noth I, Vij R, Strek ME (2016) Characterisation of patients with interstitial pneumonia with autoimmune features. Eur Respir J 47:1767–1775

    Article  CAS  Google Scholar 

  12. Chartrand S, Swigris JJ, Stanchev L, Lee JS, Brown KK, Fischer A (2016) Clinical features and natural history of interstitial pneumonia with autoimmune features: a single center experience. Respir Med 119:150–154

    Article  Google Scholar 

  13. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Norman FJF, Cooper NS, Healay LA, Kaplan SR, Laing MH, Luthra HS, Medsger TA, Michell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG (1988) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324

    Article  CAS  Google Scholar 

  14. Bohan A, Peter JB (1975) Polymyositis and dermatomyositis (first of two parts). N Engl J Med 292:344–347

    Article  CAS  Google Scholar 

  15. Masi AT (1980) Preliminary criteria for the classification of systemic sclerosis (scleroderma) Subcommittee for scleroderma criteria of the American rheumatism association diagnostic and therapeutic criteria committee. Arthritis Rheum 23:581–590

    Article  Google Scholar 

  16. Tan EM, Cohen AS, Fries JF, Masi AT, Mc Shane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277

    Article  CAS  Google Scholar 

  17. Shiboski SC, Shiboski CH, Criswell L, Baer AN, Challacombe S, Lanfranchi H, Schiedt M, Umehara H, Vivino F, Zhao Y, Dong Y, Greenspan D, Heidenriech AM, Helin P, Kirkham B, Kitagawa K, Larkin G, Li M, Lietman T, Lindegaard J, McNamara N, Sack K, Shirlaw P, Sugai S, Vollenweider C, Whitcher J, Wu A, Zhang S, Zhang W, Greenspan JS, Daniels TE (2012) Sjogren’s international collaborative clinical Alliance research G, American College of rheumatology classification criteria for Sjogren’s syndrome: a data-driven, expert consensus approach in the Sjogren’s international collaborative clinical Alliance cohort. Arthritis Care Res (Hoboken) 64:475–487

    Article  CAS  Google Scholar 

  18. Alarcon-Segovia D (1994) Mixed connective tissue disease and overlap syndromes. Clin Dermatol 12:309–316

    Article  CAS  Google Scholar 

  19. Jennette JC, Falk RJ, Andrassy K, Bacon PA, Churg J, Gross WL, Hagen EC, Hoffman GS, Hunder GG, Kallenderg CG, McCluskey RT, Sinico A, Rees AJ, van Es LA, Waldherr R, Wiik A (1994) Nomenclature of systemic vasculitides. Proposal of an international consensus conference. Arthritis Rheum 37:187–192

    Article  CAS  Google Scholar 

  20. Yoshimura K, Kono M, Enomoto Y, Nishimoto K, Oyama Y, Yasui H, Hozumi H, Karayama M, Suzuki Y, Furuhashi K, Enomoto N, Fujisawa T, Nakamura Y, Inui N, Sumikawa H, Johkoh T, Colby TV, Sugimura H, Suda T (2018) Distinctive characteristics and prognostic significance of interstitial pneumonia with autoimmune features in patients with chronic fibrosing interstitial pneumonia. Respir Med 137:167–175

    Article  Google Scholar 

  21. 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 JP, Paterson I, Filipchuk NG, Kumar A, Pauschinger M, Liuet P (2009) International consensus group on cardiovascular magnetic resonance in myocarditis, cardiovascular magnetic resonance in myocarditis: a JACC white paper. J Am Coll Cardiol 53:1475–1487

    Article  Google Scholar 

  22. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J (2005) Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol 45:1815–1822

    Article  Google Scholar 

  23. Bossuyt X, De Langhe E, Borghi MR, Meroni PL (2020) Understanding and interpreting antinuclear antibody tests in systemic rheumatic diseases. Nat Rev Rheumatol 16:715–726

    Article  CAS  Google Scholar 

  24. Pineton de Chambrun M, Charuel JL, Hekimian G, Lifermann F, Mathian A, Cohen-Aubart F, Melki I, Luyt CE, Combes A, Amoura Z (2020) Severe viral myopericarditis with autoantibodies directed against RNA polymerase III. Ann Intern Med 172:502–504

    Article  Google Scholar 

  25. 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 212:63–69

    Article  Google Scholar 

  26. Al C, Calabrese F, Angelini A, Tona F, Vinci A, Bottaro S, Ramondo A, Carturan E, Iliceto S, Thiene G, Daliento L (2007) A prospective study of biopsy-proven myocarditis: prognostic relevance of clinical and aetiopathogenetic features at diagnosis. Eur Heart J 28:1326–1333

    Article  Google Scholar 

  27. Grün S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, Kispert EM, 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

    Article  Google Scholar 

  28. Peretto G, Sala S, De Luca G, Campochiaro C, Sartorelli S, Cappelletti AM, Rizzo S, Palmisano A, Esposito A, Margonato A, Tresoldi M, Thiene G, Basso C, Dagna L, Della Bella P (2019) Impact of systemic immune-mediated diseases on clinical features and prognosis of patients with biopsy-proved myocarditis. Int J Cardiol 280:110–116

    Article  Google Scholar 

  29. Selmi C, Ceribelli A, Generali E, Scire CA, Alborghetti F, Colloredo G, Parrati L, Achenza MIS, De Santis M, Cavacioccji F, Massarotti M, Isailovic N, Paleari V, Invernizzi P, Matthias T, Zucchi A, Meroni PL (2016) Serum antinuclear and extractable nuclear antigen antibody prevalence and associated morbidity and mortality in the general population over 15 years. Autoimmun Rev 15:162–166

    Article  Google Scholar 

  30. Zawadowski GM, Klarich KW, Moder KG, Edwards W, Cooper LTJ (2012) A contemporary case series of lupus myocarditis. Lupus 21:1378–1384

    Article  CAS  Google Scholar 

  31. Pulerwitz TC, Cappola TP, Felker GM, Hare JM, Baughman KL, Kasper EK (2004) Mortality in primary and secondary myocarditis. Am Heart J 147:746–750

    Article  Google Scholar 

  32. Simpson KE, Cunningham MW, Lee CK, Ward K, Tong A, Danon S, Simon C, Delaney JW, Canter CE (2016) Autoimmunity against the heart and cardiac myosin in children with myocarditis. J Card Fail 22:520–528

    Article  CAS  Google Scholar 

  33. Ryabkova VA, Shubik YV, Erman MV, Churilov LP, Kanduc D, Shoenfeld Y (2019) Lethal immunoglobulins: autoantibodies and sudden cardiac death. Autoimmun Rev 18:415–425

    Article  CAS  Google Scholar 

  34. Allanore Y, Vignaux O, Arnaud L, Puechal X, Duboc D, Legmann P, Kahan A (2006) Effects of corticosteroids and immunosuppressors on idiopathic inflammatory myopathy related myocarditis evaluated by magnetic resonance imaging. Ann Rheum Dis 65:249–252

    Article  CAS  Google Scholar 

  35. 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. J Am Coll Cardiol 72:3158–3176

    Article  Google Scholar 

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Acknowledgements

We would like to thank Mrs. Suzanne RANKIN for editing and proofreading the manuscript.

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Authors and Affiliations

  1. Department of Cardiology, Dijon-Bourgogne University Hospital, 14 rue Gaffarel, 21079, Dijon Cedex, France

    Céline Lairet, Thibaut Pommier, Thibault Leclercq, Maud Maza, Adrien Artus & Yves Cottin

  2. Department of Internal Medicine, Dijon-Bourgogne University Hospital, 14 rue Gaffarel, 21079, Dijon Cedex, France

    Hélène Greigert, Maxime Samson & Bernard Bonnotte

  3. Department of Imagery, Dijon-Bourgogne University Hospital, 14 rue Gaffarel, 21079, Dijon Cedex, France

    Thibault Leclercq & Alexandre Cochet

  4. PEC2 Research Team, EA 7460, Department of Health Sciences, University of Burgundy, 21079, Dijon Cedex, France

    Marianne Zeller

  5. Department of Cardiology, University Teaching Hospital of Trousseau and EA7505, University François Rabelais, 37000, Tours, France

    Thibaud Genet & Laurent Fauchier

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  1. Céline Lairet
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Correspondence to Yves Cottin.

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Conflict of Interest

CL: none. HG: none. TP: none. TL: none. MM: none. AA: none. MS: no relevant COI related to the study. Roche-Chugaï (invitation to congress, personnel fees for symposium and boards), Abbvie (consulting). MZ: research grants from Amarin Corp. AC: none. BB: none. YC: no relevant COI related to the study; consultant or speaker for Bayer, BMS/Pfizer, Boehringer Ingelheim, Novartis, Sanofi and Servier.

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Lairet, C., Greigert, H., Pommier, T. et al. Acute myocarditis with autoimmune features: one-year follow-up with CMR. Heart Vessels 37, 291–299 (2022). https://doi.org/10.1007/s00380-021-01917-9

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