Established and novel treatment options in acute myocarditis, with or without heart failure

Expert Review of Cardiovascular Therapy

Volumn 15, Issue 1, 2017, Pages 25-34

  Lazaros, George ^a   Oikonomou, Evangelos ^a   Tousoulis, Dimitris ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Acute myocarditis; dilated cardiomyopathy; heart failure; infective cardiomyopathy; inflammatory cardiomyopathy; novel therapies; treatment options

Indexed keywords

ACICLOVIR; AZATHIOPRINE; CYCLOSPORIN; FOSCARNET; GANCICLOVIR; IMMUNOGLOBULIN;

ANTIRETROVIRAL THERAPY; ANTIVIRAL THERAPY; CONGESTIVE CARDIOMYOPATHY; DISEASE COURSE; EVIDENCE BASED PRACTICE; HEART EJECTION FRACTION; HEART FAILURE; HEART HEMODYNAMICS; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE BIOPSY; HOSPITAL ADMISSION; HUMAN; IMMUNOADSORPTION; IMMUNOSUPPRESSIVE TREATMENT; LONG TERM CARE; MYOCARDITIS; PATIENT REFERRAL; PERSONALIZED MEDICINE; PRACTICE GUIDELINE; PROGNOSIS; REVIEW; TREATMENT OUTCOME; VACCINATION; VIRUS GENOME; VIRUS REPLICATION; ACUTE DISEASE; BIOPSY; CARDIAC MUSCLE; CARDIOMYOPATHY, DILATED; COMPLICATION; DISEASE MANAGEMENT; HEMODYNAMICS; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ACUTE DISEASE; BIOPSY; CARDIOMYOPATHY, DILATED; DISEASE MANAGEMENT; DISEASE PROGRESSION; HEART FAILURE; HEMODYNAMICS; HUMANS; MYOCARDITIS; MYOCARDIUM;

EID: 85006317867     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1080/14779072.2017.1262764     Document Type: Review

References (85)

1. Caforio AL, Pankuweit S, Arbustini E, et al. 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. 2013;34:2636–2648.•• This article is a very useful consensus provided by European experts on the diagnosis and treatment of acute myocarditis.
2. Liu PP, Schultheiss HP., Myocarditis. In:Braunwald, Editor. Heart Disease. Philadelphia:W B Saunders Co.; 2008. p. 1775–1792.
3. Pinto YM, Elliott PM, Arbustini E, et al. Proposal for a revised definition of dilated cardiomyopathy, hypokinetic non-dilated cardiomyopathy, and its implications for clinical practice:a position statement of the ESC working group on myocardial and pericardial diseases. Eur Heart J. 2016;37:1850–1858.•• Educational article dealing with the whole spectrum of myocarditis. The proposed diagnostic and therapeutic algorithm for suspected myocarditis is a very useful guide for clinicians.
4. Adler Y, Charron P, Imazio M, et al. ESC guidelines for the diagnosis and management of pericardial diseases:the task force for the diagnosis and management of pericardial diseases of the European Society of Cardiology (ESC). Eur Heart J. 2015;36:2921–2964.
5. Sagar S, Liu PP, Cooper LT, Jr. Myocarditis. Lancet. 2012;379:738–747.
6. Shauer A, Gotsman I, Keren A, et al. Acute viral myocarditis:current concepts in diagnosis and treatment. Isr Med Assoc J. 2013;15:180–185.
7. Monti L, Moro C, Occhi L, et al. Beta blockers for haemodynamically stable acute myocarditis. J Cardiovasc Magn Reson. 2014;16(Suppl 1):P277.
8. Kindermann I, Barth C, Mahfoud F, et al. Update on myocarditis. J Am Coll Cardiol. 2012;59:779–792.
9. Mirabel M, Luyt CE, Leprince P, et al. Outcomes, long-term quality of life, and psychologic assessment of fulminant myocarditis patients rescued by mechanical circulatory support. Crit Care Med. 2011;39:1029–1035.
10. Chen YS, Wang MJ, Chou NK, et al. Rescue for acute myocarditis with shock by extracorporeal membrane oxygenation. Ann Thorac Surg. 1999;68:2220–2224.
11. Hsu KH, Chi NH, Yu HY, et al. Extracorporeal membranous oxygenation support for acute fulminant myocarditis:analysis of a single center’s experience. Eur J Cardiothorac Surg. 2011;40:682–688.
12. McNamara DM, Holubkov R, Starling RC, et al. Controlled trial of intravenous immune globulin in recent-onset dilated cardiomyopathy. Circulation. 2001;103:2254–2259.
13. Cooper L. Myocarditis. N Engl J Med. 2009;360(1526–1538):1526–1538.•• A comprehensive overview on the pathogenesis, clinical course, and treatment of acute myocarditis.
14. McCarthy RE, Boehmer JP, Hruban RH, et al. Long-term outcome of fulminant myocarditis as compared with acute (non fulminant) myocarditis. N Engl J Med. 2000;342:690–695.
15. Cooper LT, Jr, Berry GJ, Shabetai R. Idiopathic giant-cell myocarditis–natural history and treatment. Multicenter giant cell myocarditis study group investigators. N Engl J Med. 1997;336:1860–1866.
16. Gupta S, Markham DW, Drazner MH, et al. Fulminant myocarditis. Nat Clin Pract Cardiovasc Med. 2008;5:693–706.
17. Cooper LT, Baughman KL, Feldman AM, et al. The role of endomyocardial biopsy in the management of cardiovascular disease:a scientific statement from the American heart association, the American college of cardiology, and the European society of cardiology. Circulation. 2007;116:2216–2233.
18. Li H, Dai Z, Wang B, et al. A case report of eosinophilic myocarditis and a review of the relevant literature. BMC Cardiovasc Disord. 2015;15:15.
19. Gkouziouta A, Miliopoulos D, Karavolias G, et al. Acute cytomegalovirus infection triggering fatal giant cell myocarditis. Int J Cardiol. 2016;214:204–206.
20. Ekström K, Lehtonen J, Kandolin R, et al. Long-term outcome and its predictors in giant cell myocarditis. Eur J Heart Fail. 2016 Jul;13. DOI:10.1002/ejhf.606,
21. Kandolin R, Lehtonen J, Salmenkivi K, et al. Diagnosis, treatment, and outcome of giant-cell myocarditis in the era of combined immunosuppression. Circ Heart Fail. 2013;6:15–22.
22. Menghini VV, Savcenko V, Olson LJ, et al. Combined immunosuppression for the treatment of idiopathic giant cell myocarditis. Mayo Clin Proc. 1999;74:1221–1226.
23. Ponikowski P, Voors AA, Anker SD, et al. 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. Eur Heart J. 2016;2016(37):2129–2200.
24. Writing committee members; ACC/AHA TASK FORCE members. 2016. ACC/AHA/HFSA Focused Update on New Pharmacological Therapy for Heart Failure:An Update of the 2013 ACCF/AHA Guideline for the Management of Heart Failure:A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Failure Society of America. J Card Fail. 2016;22:659-669.
25. Veeraveedu PT, Watanabe K, Ma M, et al. Torasemide, a long acting loop diuretic, reduces the progression of myocarditis to dilated cardiomyopathy. Eur J Pharmacol. 2008;581:121–131.
26. Kindermann I, Kindermann M, Kandolf R, et al. Predictors of outcome in patients with suspected myocarditis. Circulation. 2008;118:639–648.
27. Feldman AM, McNamara D. Myocarditis. N Engl J Med. 2000;343(1388–1398):1388–1398.
28. Tominaga M, Matsumori A, Okada I, et al. Beta-blocker treatment of dilated cardiomyopathy:beneficial effect of carteolol in mice. Circulation. 1991;83:2021–2028.
29. Yuan Z, Shioji K, Kihara Y, et al. Cardioprotective effects of carvedilol on acute autoimmune myocarditis:anti-inflammatory effects associated with antioxidant property. Am J Physiol Heart Circ Physiol. 2004;286:H83–H90.
30. Rezkalla S, Kloner RA, Khatib G, et al. Effect of metoprolol in acute coxsackievirus B3 murine myocarditis. J Am Coll Cardiol. 1988;12:412–414.
31. Saegusa S, Fei Y, Takahashi T, et al. Oral administration of candesartan improves the survival of mice with viral myocarditis through modification of cardiac adiponectin expression. Cardiovasc Drugs Ther. 2007;21:155–160.
32. Bahk TJ, Daniels MD, Leon JS, et al. Comparison of angiotensin converting enzyme inhibition and angiotensin II receptor blockade for the prevention of experimental autoimmune myocarditis. Int J Cardiol. 2008;125:85–93.
33. Sukumaran V, Watanabe K, Veeraveedu PT, et al. Beneficial effects of olmesartan, an angiotensin II receptor type 1 antagonist, in rats with dilated cardiomyopathy. Exp Biol Med. (Maywood). 2010;235:1338–1346.
34. Reyes MP, Khatib R, Khatib G, et al. Prolonged captopril therapy in murine viral myocarditis. J Cardiovasc Pharmacol Ther. 1998;3:43–50.
35. Seko Y. Effect of the angiotensin II receptor blocker olmesartan on the development of murine acute myocarditis caused by coxsackievirus B3. Clin Sci (Lond). 2006;110:379–386.
36. Araki M, Kanda T, Imai S, et al. Comparative effects of losartan, captopril, and enalapril on murine acute myocarditis due to encephalomyocarditis virus. J Cardiovasc Pharmacol. 1995;26:61–65.
37. Xiao J, Shimada M, Liu W, et al. Antiinflammatory effects of eplerenone on viral myocarditis. Eur J Heart Fail. 2009;11:349–353.
38. Anguita-Sánchez M, Castillo-Domínguez JC, Mesa-Rubio D, et al. Should angiotensin-converting enzyme inhibitors be continued over the long term in patients whose left ventricular ejection fraction normalizes after an episode of acute myocarditis? Rev Esp Cardiol. 2006;59:1199–1201.
39. Dennert R, Crijns HJ, Heymans S. Acute viral myocarditis. Eur Heart J. 2008;29:2073–2082.•• Valuable summary of acute viral myocarditis.
40. Karavidas A, Lazaros G, Noutsias M, et al. Recurrent coxsackie B viral myocarditis leading to progressive impairment of left ventricular function over 8 years. Int J Cardiol. 2011;151:e65–e7.
41. Veeraveedu PT, Watanabe K, Ma M, et al. Comparative effects of pranidipine with amlodipine in rats with heart failure. Pharmacology. 2006;77:1–10.
42. Liu W, Shimada M, Xiao J, et al. Nifedipine inhibits the activation of inflammatory and immune reactions in viral myocarditis. Life Sci. 2009;85:235–240.
43. Canter CE, Simpson KE. Diagnosis and treatment of myocarditis in children in the current era. Circulation. 2014;129:115–128.
44. Matsumori A, Igata H, Ono K, et al. High doses of digitalis increase the myocardial production of proinflammatory cytokines and worsen myocardial injury in viral myocarditis:a possible mechanism of digitalis toxicity. Jpn Circ J. 1999;63:934–940.
45. Costanzo-Nordin MR, Reap EA, O’Connell JB, et al. A non-steroidal anti-inflammatory drug exacerbates coxsackie B3 murine myocarditis. J Am Coll Cardiol. 1985;6:1078–1082.
46. Khatib R, Reyes MP, Smith F, et al. Enhancement of coxsackievirus B4 virulence by indomethacin. J Lab Clin Med. 1990;116:116–120.
47. Khatib R, Reyes MP, Smith FE. Enhancement of coxsackievirus B3 replication in vero cells by indomethacin. J Infect Dis. 1990;162:997–998.
48. Blauwet LA, Cooper LT. Myocarditis. Prog Cardiovasc Dis. 2010;52:274–288.
49. Friedrich MG, Sechtem U, Schulz-Menger J, et al. International consensus group on cardiovascular magnetic resonance in myocarditis. Cardiovascular magnetic resonance in myocarditis:a JACC white paper. J Am Coll Cardiol. 2009;53:1475–1487.
50. Imazio M, Brucato A, Barbieri A, et al. Good prognosis for pericarditis with and without myocardial involvement:results from a multicenter, prospective cohort study. Circulation. 2013;128:42–49.
51. Imazio M, Cooper LT. Management of myopericarditis. Expert Rev Cardiovasc Ther. 2013;11:193–201.
52. Imazio M, Brucato A, Forno D, et al. Efficacy and safety of colchicine for pericarditis prevention. Systematic review and meta-analysis. Heart. 2012;98:1078–1082.
53. Dubrey SW, Falk RH. Diagnosis and management of cardiac sarcoidosis. Prog Cardiovasc Dis. 2010;52:336–346.
54. Priori SG, Blomström-Lundqvist C, Mazzanti A, et al. ESC Guidelines for the management of patients with ventricular arrhythmias and the prevention of sudden cardiac death. Eur Heart J. 2015;2015(36):2793–2867.
55. Aziz S, Leon AR, El-Chami MF. The subcutaneous defibrillator:a review of the literature. J Am Coll Cardiol. 2014;63:1473–1479.
56. Ali H, Lupo P, Cappato R. The entirely subcutaneous defibrillator - A new generation and future expectations. Arrhythm Electrophysiol Rev. 2015;4:116–121.
57. Mason JW, O Connell JB, Herskowitz A, et al. A clinical trial of immunosuppressive therapy for myocarditis. N Engl J Med. 1995;333:269–275.
58. Frustaci A, Russo MA, Chimenti C. Randomized study on the efficacy of immunosuppressive therapy in patients with virus-negative inflammatory cardiomyopathy:the TIMIC study. Eur Heart J. 2009;30:1995–2002.
59. Adamopoulos S, Gkouziouta A, Lazaros G, et al. Endomyocardial biopsy in new onset dilated cardiomyopathy:prevalence and prognostic role of infectious agents. Int J Cardiol. 2013;168:e129–e30.
60. Wojnicz R, Nowalany-Kozielska E, Wojciechowska C, et al. Randomized, placebo-controlled study for immunosuppressive treatment of inflammatory dilated cardiomyopathy:two-year follow-up results. Circulation. 2001;104:39–45.
61. Caforio AL, Calabrese F, Angelini A, et al. A prospective study of biopsy-proven myocarditis:prognostic relevance of clinical and aetiopathogenetic features at diagnosis. Eur Heart J. 2007;28:1326–1333.
62. Pollack A, Kontorovich AR, Fuster V, et al. Viral myocarditis–diagnosis, treatment options, and current controversies. Nat Rev Cardiol. 2015;12:670–680.
63. Gkouziouta A, Lazaros G, Karavidas A, et al. Pathogen-driven treatment strategy in new onset dilated cardiomyopathy. Impact on ventricular function and clinical outcome. Int J Cardiol. 2016;209:15–16.• This is the first study evaluating the impact of pathogen-driven treatment in the long term.
64. Schultheiss HP, Kuhl U, Cooper LT. The management of myocarditis. Eur Heart J. 2011;32:2616–2625.•• Comprehensive and detailed description of the progression of myocarditis to the various forms of cardiomyopathy.
65. Mavrogeni S, Markousis-Mavrogenis G, Kolovou G. How to approach the great mimic? Improving techniques for the diagnosis of myocarditis. Expert Rev Cardiovasc Ther. 2016;14:105–115.
66. Kuhl U, Pauschinger M, Schwimmbeck PL, et al. Interferon beta treatment eliminates cardiotropic viruses and improves left ventricular function in patients with myocardial persistence of viral genomes and left ventricular dysfunction. Circulation. 2003;107:2793–2798.
67. Schultheiss HP, Piper C, Sowade K, et al. The effect of subcutaneous treatment with interferon-beta-1b over 24 weeks on safety, virus elimination and clinical outcome in patients with chronic viral cardiomyopathy (abstr). Circulation. 2008;118:3322.
68. Imazio M, Lazaros G, Brucato A, et al. Recurrent pericarditis:new and emerging therapeutic options. Nat Rev Cardiol. 2016;13:99–105.
69. Robinson J, Hartling L, Vandermeer B, et al. Intravenous immunoglobulin for presumed viral myocarditis in children and adults. Cochrane Database Syst Rev. 2015 May 20;(5):CD004370. doi:10.1002/14651858.
70. Drucker NA, Colan SD, Lewis AB, et al. Gamma-globulin treatment of acute myocarditis in the pediatric population. Circulation. 1994;89:252–257.
71. Di Filippo S. Improving outcomes of acute myocarditis in children. Expert Rev Cardiovasc Ther. 2016;14:117–125.
72. Felix SB, Beug D, Dörr M. Immunoadsorption therapy in dilated cardiomyopathy. Expert Rev Cardiovasc Ther. 2015;13:145–152.
73. Lazaros G, Karavidas A, Spyropoulou M, et al. The role of the immunogenetic background in the development and recurrence of acute idiopathic pericarditis. Cardiology. 2011;118:55–62.
74. Huber SA. Autoimmunity in myocarditis:relevance of animal models. Clin Immunol Immunopathol. 1997;83:93–102.
75. Matsumori A. Emerging treatments for viral myocarditis. Future Cardiol. 2005;1:683–692.• This review summarizes the novel treatment options in the context of viral myocarditis.
76. Coronado MJ, Brand JE, Kim E, et al. Testosterone and interleukin-1β increase cardiac remodeling during coxsackievirus B3 myocarditis via serpin A 3n. Am J Physiol Circ Physiol. 2012;302:H1726–H1736.
77. Jensen LD, Marchant DJ. Emerging pharmacologic targets and treatments for myocarditis. Pharmacol Ther. 2016;161:40–51.
78. Nugent AW, Daubeney PE, Chondros P, et al. National Australian childhood cardiomyopathy study. The epidemiology of childhood cardiomyopathy in Australia. N Engl J Med. 2003;348:1639–1646.
79. Corsten N, Papageorgiou A, Verhesen W, et al. MicroRNA profiling identifies microRNA-155 as an adverse mediator of cardiac injury and dysfunction during acute viral myocarditis. Circ Res. 2012;111:415–425.• This paper highlights the role of micro-RNA as mediators of cardiac injury and dysfunction during acute viral myocarditis.
80. Magnani J, Dec W. Myocarditis:Current Trends in Diagnosis and Treatment Circulation. 2006;113:876–890.
81. Mahrholdt H, Wagner A, Deluigi CC, et al. Presentation, patterns of myocardial damage and clinical course of viral myocarditis. Circulation. 2006;114:1581–1590.• Detailed review of the contemporary trends on diagnostic procedures and treatment options in myocarditis.
82. Cooper LT., The natural history and role of immunoadsorption in dilated cardiomyopathy. J Clin Apher. 2005;20:256–260.
83. Liu P, Mason J. Advances in the understanding of myocarditis. Circulation. 2001;104:1076–1082.
84. Basso C, Carturan E, Corrado D, et al. Myocarditis and dilated cardiomyopathy in athletes:diagnosis, management and recommendations for sport activity. Cardiol Clin. 2007;25:423–429.
85. Pelliccia A, Fagard R, Bjørnstad HH, et al. Recommendations for competitive sports participation in athletes with cardiovascular disease:a consensus document from the study group of sports cardiology of the working group of cardiac rehabilitation and exercise physiology and the working group of myocardial and pericardial diseases of the European society of cardiology. Eur Heart J. 2005;26:1422–1445.