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Cooper","issue_and_volume":"Volume 32 | Issue 21","type":"review-article","online_publication_date":"2011-06-23","access_type":"Free","license_type":"free","event_type":"full-text","supplier_tag":"SC_Journals","object_type":"Article","taxonomy":"taxId%3a39%7ctaxLabel%3aAcademicSubjects%7cnodeId%3aMED00200%7cnodeLabel%3aCardiovascular+Medicine%7cnodeLevel%3a3","siteid":"eurheartj","authzrequired":"false","doi":"10.1093/eurheartj/ehr165"}]; </script> <script> (function (w, d, s, l, i) { w[l] = w[l] || []; w[l].push({ 'gtm.start': new Date().getTime(), event: 'gtm.js' }); var f = d.getElementsByTagName(s)[0], j = d.createElement(s), dl = l != 'dataLayer' ? 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Despite considerable advances in our understanding of myocarditis pathogenesis, the clinical management of myocarditis has changed relatively lit","pageStart":"2616","pageEnd":"2625","siteName":"OUP Academic","thumbnailURL":"https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1794577257&Signature=ZinKADomBSRNdw-IUxT-GXU-Na-xjsojnofnBUAYccsaTvrfhfXI4SnyNpJTzaSZxhXsKT9xWkUiJ0N14~TknHnMMgXPYPkHByk~UK-f5Rrmx-7cGLTaZEo6Dqx--6gcc4pfS1HJjDBtCqeyIYoxiuHXut-LlEloiDU-oNHb0hh4PYuWbgZJo59swcsIcu-h4z0PXgvNXCZOUMN8tkfuw-Prb8M-0w9P7b0JSIXAPHApWwmyZp2OAN00WLj16adlMQOYaEj4DL8Xd02EfJXWeS1~eoy6psIaW2stXJnBf4boBlG~ntHIb~1m3rUtP26bZbPPwtABGwP4ASE5UW5qZA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA","headline":"The management of myocarditis","image":"https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1794577257&Signature=ZinKADomBSRNdw-IUxT-GXU-Na-xjsojnofnBUAYccsaTvrfhfXI4SnyNpJTzaSZxhXsKT9xWkUiJ0N14~TknHnMMgXPYPkHByk~UK-f5Rrmx-7cGLTaZEo6Dqx--6gcc4pfS1HJjDBtCqeyIYoxiuHXut-LlEloiDU-oNHb0hh4PYuWbgZJo59swcsIcu-h4z0PXgvNXCZOUMN8tkfuw-Prb8M-0w9P7b0JSIXAPHApWwmyZp2OAN00WLj16adlMQOYaEj4DL8Xd02EfJXWeS1~eoy6psIaW2stXJnBf4boBlG~ntHIb~1m3rUtP26bZbPPwtABGwP4ASE5UW5qZA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA","image:alt":"Distinct phases of myocardial injury in infectious and post-infectious myocarditis. Myocarditis is an inﬂammatory disease of the cardiac muscle caused by myocardial inﬁltration of immunocompetent cells following any kind of cardiac injury. Acute myocarditis is often a result of a viral infection that produces myocardial necrosis and triggers an immune response to eliminate the infectious agent (healed myocarditis and/or dilated cardiomyopathy). Chronic myocardial injury may be caused by post-infectious immune or autoimmune processes [indlammatory cardiomyopathy (DCMi)], be associated with systemic autoimmune diseases or develop by a persisting virus infection (viral heart disease), which, in the long run, are responsible for persistent or progressive ventricular dysfunction, arrhythmias, and cardiac complaints. The disease often presents as an acute form of dilated cardiomyopathy but due to its broad spectrum of presentation the clinical diagnosis is frequently misleading. If the underlying infectious or immune-mediated causes of the disease are carefully defined by clinical and biopsy-based tools, specific immunosuppressive and antiviral treatment options in addition to basic symptomatic therapy may improve prognosis in a number of patients with acute and chronic disease."} </script> <meta property="og:site_name" content="OUP Academic" /> <meta property="og:title" content="The management of myocarditis" /> <meta property="og:description" content="Abstract. Despite considerable advances in our understanding of myocarditis pathogenesis, the clinical management of myocarditis has changed relatively lit" /> <meta property="og:type" content="article" /> <meta property="og:url" content="https://dx.doi.org/10.1093/eurheartj/ehr165" /> <meta property="og:updated_time" content="" /> <meta property="og:image" content="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1794577257&Signature=ZinKADomBSRNdw-IUxT-GXU-Na-xjsojnofnBUAYccsaTvrfhfXI4SnyNpJTzaSZxhXsKT9xWkUiJ0N14~TknHnMMgXPYPkHByk~UK-f5Rrmx-7cGLTaZEo6Dqx--6gcc4pfS1HJjDBtCqeyIYoxiuHXut-LlEloiDU-oNHb0hh4PYuWbgZJo59swcsIcu-h4z0PXgvNXCZOUMN8tkfuw-Prb8M-0w9P7b0JSIXAPHApWwmyZp2OAN00WLj16adlMQOYaEj4DL8Xd02EfJXWeS1~eoy6psIaW2stXJnBf4boBlG~ntHIb~1m3rUtP26bZbPPwtABGwP4ASE5UW5qZA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" /> <meta property="og:image:url" content="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1794577257&Signature=ZinKADomBSRNdw-IUxT-GXU-Na-xjsojnofnBUAYccsaTvrfhfXI4SnyNpJTzaSZxhXsKT9xWkUiJ0N14~TknHnMMgXPYPkHByk~UK-f5Rrmx-7cGLTaZEo6Dqx--6gcc4pfS1HJjDBtCqeyIYoxiuHXut-LlEloiDU-oNHb0hh4PYuWbgZJo59swcsIcu-h4z0PXgvNXCZOUMN8tkfuw-Prb8M-0w9P7b0JSIXAPHApWwmyZp2OAN00WLj16adlMQOYaEj4DL8Xd02EfJXWeS1~eoy6psIaW2stXJnBf4boBlG~ntHIb~1m3rUtP26bZbPPwtABGwP4ASE5UW5qZA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" /> <meta property="og:image:secure_url" content="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1794577257&Signature=ZinKADomBSRNdw-IUxT-GXU-Na-xjsojnofnBUAYccsaTvrfhfXI4SnyNpJTzaSZxhXsKT9xWkUiJ0N14~TknHnMMgXPYPkHByk~UK-f5Rrmx-7cGLTaZEo6Dqx--6gcc4pfS1HJjDBtCqeyIYoxiuHXut-LlEloiDU-oNHb0hh4PYuWbgZJo59swcsIcu-h4z0PXgvNXCZOUMN8tkfuw-Prb8M-0w9P7b0JSIXAPHApWwmyZp2OAN00WLj16adlMQOYaEj4DL8Xd02EfJXWeS1~eoy6psIaW2stXJnBf4boBlG~ntHIb~1m3rUtP26bZbPPwtABGwP4ASE5UW5qZA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" /> <meta property="og:image:alt" content="Distinct phases of myocardial injury in infectious and post-infectious myocarditis. Myocarditis is an inﬂammatory disease of the cardiac muscle caused by myocardial inﬁltration of immunocompetent cells following any kind of cardiac injury. Acute myocarditis is often a result of a viral infection that produces myocardial necrosis and triggers an immune response to eliminate the infectious agent (healed myocarditis and/or dilated cardiomyopathy). Chronic myocardial injury may be caused by post-infectious immune or autoimmune processes [indlammatory cardiomyopathy (DCMi)], be associated with systemic autoimmune diseases or develop by a persisting virus infection (viral heart disease), which, in the long run, are responsible for persistent or progressive ventricular dysfunction, arrhythmias, and cardiac complaints. The disease often presents as an acute form of dilated cardiomyopathy but due to its broad spectrum of presentation the clinical diagnosis is frequently misleading. If the underlying infectious or immune-mediated causes of the disease are carefully defined by clinical and biopsy-based tools, specific immunosuppressive and antiviral treatment options in addition to basic symptomatic therapy may improve prognosis in a number of patients with acute and chronic disease." /> <meta name="twitter:card" content="summary_large_image" /> <meta name="citation_author" content="Schultheiss, Heinz-Peter" /><meta name="citation_author_institution" content="Charite Hospital, Berlin, Germany" /><meta name="citation_author_institution" content="Mayo Clinic, Rochester, MN, USA" /><meta name="citation_author" content="Kühl, Uwe" /><meta name="citation_author_institution" content="Charite Hospital, Berlin, Germany" /><meta name="citation_author_institution" content="Mayo Clinic, Rochester, MN, USA" /><meta name="citation_author" content="Cooper, Leslie T." /><meta name="citation_author_institution" content="Charite Hospital, Berlin, Germany" /><meta name="citation_author_institution" content="Mayo Clinic, Rochester, MN, USA" /><meta name="citation_title" content="The management of myocarditis" /><meta name="citation_firstpage" content="2616" /><meta name="citation_lastpage" content="2625" /><meta name="citation_doi" content="10.1093/eurheartj/ehr165" /><meta name="citation_keyword" content="myocarditis" /><meta name="citation_keyword" content="viruses" /><meta name="citation_journal_title" content="European Heart Journal" /><meta name="citation_journal_abbrev" content="Eur Heart J" /><meta name="citation_volume" content="32" /><meta name="citation_issue" content="21" /><meta name="citation_publication_date" content="2011/11/01" /><meta name="citation_issn" content="0195-668X" /><meta name="citation_publisher" content="Oxford Academic" /><meta name="citation_reference" content="citation_title=Myocarditis related to drug hypersensitivity; Mayo Clin Proc; citation_year=1985; citation_volume=60; citation_pages=463-468; " /><meta name="citation_reference" content="citation_title=Histopathologic and immunohistochemical features of fatal influenza virus infection in children during the 2003–2004 season; Clin Infect Dis; citation_year=2006; citation_volume=43; citation_pages=132-140; " /><meta name="citation_reference" content="citation_title=Myocarditis; citation_edition=8th ed.; citation_publisher=W B Saunders Co, Philadelphia; Heart Disease; citation_year=2008; citation_pages=1775-1792; " /><meta name="citation_reference" content="citation_title=Myocarditis; Prog Cardiovasc Dis; citation_year=2010; citation_volume=52; citation_pages=274-288; " /><meta name="citation_reference" content="citation_title=Molecular diagnosis of myocarditis and dilated cardiomyopathy in children: clinicopathologic features and prognostic implications; Diagn Mol Pathol; citation_year=2002; citation_volume=11; citation_pages=212-221; " /><meta name="citation_reference" content="citation_title=The detection of viral genomes by polymerase chain reaction in the myocardium of pediatric patients with advanced HIV disease; J Am Coll Cardiol; citation_year=1999; citation_volume=34; citation_pages=857-865; " /><meta name="citation_reference" content="citation_title=Detection of viruses in myocardial tissues by polymerase chain reaction. 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<ul class="jumplink-list js-jumplink-list"> <li class="section-jump-link head-1" link-destination="6566896"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566896">Abstract</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566898"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566898">Aetiology of myocarditis</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566902"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566902">Pathogenic mechanisms</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566922"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566922">Diagnosis and prognosis</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566930"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566930">Treatment</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566947"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566947">Immunosuppression</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566952"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566952">Intravenous immunoglobulin and immunoadsorption</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566955"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566955">Summary and perspectives</a> </div> </li> <li class="section-jump-link head-1" link-destination="6566957"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566957">Funding</a> </div> </li> <li class="section-jump-link head-1 backReferenceLink" link-destination="6566963"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#6566963">References</a> </div> </li> </ul> 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class="content-inner-wrap"> <div class="widget widget-ArticleTopInfo widget-instance-OUP_ArticleTop_Info_Widget"> <div class="module-widget article-top-widget"> <div class="access-state-logos all-viewports"> <span class="journal-info__format-label">Journal Article</span> </div> <div class="widget-items"> <div class="title-wrap"> <h1 class="wi-article-title article-title-main accessible-content-title at-articleTitle"> The management of myocarditis <i class='icon-availability_free' title='Free' ></i> </h1> </div> <div class="wi-authors at-ArticleAuthors"> <div class="al-authors-list"> <span class="al-author-name-more js-flyout-wrap"> <button type="button" class="linked-name js-linked-name-trigger btn-as-link">Heinz-Peter Schultheiss</button><span class='delimiter'>, </span> <span class="al-author-info-wrap arrow-up"> <div class="info-card-author authorInfo_OUP_ArticleTop_Info_Widget"> <div class="name-role-wrap"> <div class="info-card-name"> Heinz-Peter Schultheiss <span 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Tel: +49 308 445 2344; Fax: +49 308 445 3565; Email: <a href="mailto:heinz-peter.schultheiss@charite.de" target="_blank">heinz-peter.schultheiss@charite.de</a></div> </div> <div class="info-card-search-label"> Search for other works by this author on: </div> <div class="info-card-search info-card-search-internal"> <a href="/eurheartj/search-results?f_Authors=Heinz-Peter+Schultheiss" rel="nofollow">Oxford Academic</a> </div> <div class="info-card-search info-card-search-pubmed"> <a href="http://www.ncbi.nlm.nih.gov/pubmed?cmd=search&term=Schultheiss H">PubMed</a> </div> <div class="info-card-search info-card-search-google"> <a href="http://scholar.google.com/scholar?q=author:%22Schultheiss Heinz-Peter%22">Google Scholar</a> </div> </div> </span> </span> <span class="al-author-name-more js-flyout-wrap"> <button type="button" class="linked-name js-linked-name-trigger btn-as-link">Uwe Kühl</button><span class='delimiter'>, </span> <span class="al-author-info-wrap arrow-up"> <div class="info-card-author authorInfo_OUP_ArticleTop_Info_Widget"> <div class="name-role-wrap"> <div class="info-card-name"> Uwe Kühl </div> </div> <div class="info-card-affilitation"> <div class="aff"><span class="label title-label">1</span><div class="institution">Charite Hospital</div>, <div class="addr-line">Berlin</div>, <div class="country">Germany</div></div><div class="aff"><span class="label title-label">2</span><div class="institution">Mayo Clinic</div>, <div class="addr-line">Rochester, MN</div>, <div class="country">USA</div></div> </div> <div class="info-card-search-label"> Search for other works by this author on: </div> <div class="info-card-search info-card-search-internal"> <a href="/eurheartj/search-results?f_Authors=Uwe+K%c3%bchl" rel="nofollow">Oxford Academic</a> </div> <div class="info-card-search info-card-search-pubmed"> <a href="http://www.ncbi.nlm.nih.gov/pubmed?cmd=search&term=Kühl U">PubMed</a> </div> <div class="info-card-search info-card-search-google"> <a href="http://scholar.google.com/scholar?q=author:%22Kühl Uwe%22">Google Scholar</a> </div> </div> </span> </span> <span class="al-author-name-more js-flyout-wrap"> <button type="button" class="linked-name js-linked-name-trigger btn-as-link">Leslie T. Cooper</button><span class='delimiter'></span> <span class="al-author-info-wrap arrow-up"> <div class="info-card-author authorInfo_OUP_ArticleTop_Info_Widget"> <div class="name-role-wrap"> <div class="info-card-name"> Leslie T. 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icon-menu_search"> <span class="screenreader-text">Search</span> </a> </div> </div> <div class="navbar-search-advanced"><a href="/eurheartj/advanced-search" class="advanced-search js-advanced-search">Advanced Search</a></div> </div> <div class="navbar-search-collapsed"><a href="javascript:;" class="icon-menu_search js_expand-navsearch"><span class="screenreader-text">Search Menu</span></a></div> </div> </div> <input id="routename" name="RouteName" type="hidden" value="eurheartj" /> </div> </div> </div> </div> <div id="ContentTab" class="content active"> <div class="widget widget-ArticleFulltext widget-instance-OUP_Article_FullText_Widget"> <div class="module-widget"> <div class="widget-items" data-widgetname="ArticleFulltext"> <h2 scrollto-destination=6566896 id="6566896" class="abstract-title js-splitscreen-abstract-title" >Abstract</h2> <section class="abstract"><p class="chapter-para">Despite considerable advances in our understanding of myocarditis pathogenesis, the clinical management of myocarditis has changed relatively little in the last few years. This review aims to help bridge the widening gap between recent mechanistic insights, which are largely derived from animal models, and their potential impact on disease burden. We illustrate the pathogenenic mechanisms that are prime targets for novel therapeutic interventions. Pathway and pathogen-specific molecular diagnostic tests have expanded the role for endomyocardial biopsy. State of the art cardiac magnetic resonance imaging can now provide non-invasive tissue characterization and localize inflammatory infiltrates but imaging techniques are misleading if infectious agents are involved. We emphasize the gaps in our current clinical knowledge, particularly with respect to aetiology-based therapy, and suggest opportunities for high impact, translational investigations.</p></section> <div class="article-metadata-panel clearfix at-ArticleMetadata"></div> <div class="kwd-group"><a class="kwd-part kwd-main" href="javascript:;" data-keyword=""Myocarditis pathogenesis"">Myocarditis pathogenesis</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""Clinical management"">Clinical management</a></div> <h2 scrollto-destination=6566898 id="6566898" class="section-title js-splitscreen-section-title" data-legacy-id=s1>Aetiology of myocarditis</h2> <p class="chapter-para">Aetiologies of myocarditis include a number of infectious and non-infectious agents such as viruses, bacteria, protozoa, fungi, toxins, myocardial involvement in systemic diseases, or physical condition, but often the underlying cause cannot be identified (<em>Table <span class="xrefLink" id="jumplink-EHR165TB1"></span><a href="javascript:;" reveal-id="EHR165TB1" data-open="EHR165TB1" class="link link-reveal link-table xref-fig">1</a></em>). Drugs can induce myocardial inflammation by either direct toxic effects on heart tissue or by inducing hypersensitivity reactions, which are often associated with an eosinophilic myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C1"></span><a href="javascript:;" reveal-id="EHR165C1" data-open="EHR165C1" class="link link-ref link-reveal xref-bibr">1</a></sup> Eosinophils are also observed in myocardial inflammatory processes which are associated with Churg–Strauss or hypereosinophilic syndromes, vaccination against smallpox or caused by helminthic and parasitic infections. Myocardial involvement may be caused by granulomatous and systemic diseases or (auto)immune processes with often unknown pathogenetic mechanisms, but all these aetiologies are far less common than virus-induced myocarditis or post-infectious inflammatory cardiomyopathy.<sup><span class="xrefLink" id="jumplink-EHR165C2 EHR165C4"></span><a href="javascript:;" reveal-id="EHR165C2 EHR165C4" data-open="EHR165C2 EHR165C4" class="link link-ref link-reveal xref-bibr">2–4</a></sup> Apart from enteroviruses, which traditionally have been considered the most common agent in myocarditis and dilated cardiomyopathy, distinct RNA- and DNA viruses and virus subtypes have been identified with varying degrees of frequency (<em>Table <span class="xrefLink" id="jumplink-EHR165TB1"></span><a href="javascript:;" reveal-id="EHR165TB1" data-open="EHR165TB1" class="link link-reveal link-table xref-fig">1</a></em>).<sup><span class="xrefLink" id="jumplink-EHR165C5 EHR165C22"></span><a href="javascript:;" reveal-id="EHR165C5 EHR165C22" data-open="EHR165C5 EHR165C22" class="link link-ref link-reveal xref-bibr">5–22</a></sup></p> <a id="6566900" scrollto-destination="6566900"></a> <div content-id="EHR165TB1" class="table-modal table-full-width-wrap"><div class="table-wrap table-wide standard-table"><div class="table-wrap-title" id="EHR165TB1" data-id="EHR165TB1"><span class="label title-label" id="label-17728">Table 1</span><div class="
 graphic-wrap table-open-button-wrap
 "><a class="fig-view-orig at-tableViewLarge openInAnotherWindow btn js-view-large" role="button" target="_blank" href="
 /view-large/6566900" aria-describedby="label-17728"> Open in new tab </a></div><div class="caption caption-id-" id="caption-17728"><p class="chapter-para">Causes of myocarditis</p></div> </div><div class="table-overflow"><table role="table" aria-labelledby="
 label-17728" aria-describedby="
 caption-17728"><thead><tr><th>Infectious causes<span aria-hidden="true" style="display: none;"> . </span></th><th>Non-infectious causes<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td>RNA viruses: picornaviruses (coxsackie A + B, echovirus, poliovirus, hepatitis virus), orthomyxovirus (influenza), paramyxoviruses (respiratory syncitial virus, mumps), togaviruses (rubella), flaviviruses (dengue fever, yellow fever)</td><td>Autoimmune diseases: dematomyositis, inflammatory bowel disease, rheumatoid arthritis, sjögren syndrome, systemic lupus erythematodes, Wegener's granulomatosis, giant cell myocarditis</td></tr><tr><td>DNA viruses: adenovirus (A 1, 2 ,3, and 5), erythrovirus [1 (B19V) and 2], herpesviruses (human herpes virus 6 A/B, cytomegalievirus, Epstein-Barr virus, varicella-zoster virus), retrovirus (HIV)</td><td>Drugs: aminophyllin, amphetamine, anthracyclin, catecholamines, chloramphenicol, cocain cyclophosphamid, doxorubicin, 5-fluoruracil, mesylate, methylsergit, phenytoin, trastuzumab, zidovudine</td></tr><tr><td>Bacteria: chlamydia (<em>C. pneumonia</em>/psittacosis) haemophilus influence, legionella, pneumophilia, brucella clostridium, francisella tularensis, neisseria meningitis, mycobacterium (tuberculosis), salmonella, staphylococcus, streptococcus A, S. pneumonia, tularemia, tetanus, syphilis, <em>Vibrio cholera</em></td><td>Hypersensitivity reactions (drugs): azitromycin, benzodiazepines, clozapine, cephalosporins, dapsone, dobutamin, lithium, diuretics, thiazide, methyldopa, mexiletine, Streptomycin, sulfonamides, non-steroidal anti-inflammational drugs, tetanus toxoid, tetracycline, tricyclic antidepressiva</td></tr><tr><td>Spirocheta: <em>Borrelia recurrentis</em>, leptospira, <em>Treponema pallidum</em></td><td>Hypersensitivity reactions (venomes): bee, wasp, black widow spider, scorpion, snakes</td></tr><tr><td>Reckettsia: <em>Coxiella burnetii</em>, <em>R. rickettsii</em>/<em>prowazekii</em></td><td>Systemic diseases: Churg-Strauss syndrome, collagen diseases, sarcoidosis, Kawasaki disease, scleroderma</td></tr><tr><td>Fungi: actinomyces, aspergillus, candida, cryptococcus, histoplasma, nocardia</td><td>Others: heart stroke, hypothermia, transplant rejection, radiation injury</td></tr><tr><td>Protozoa: <em>Entamoeba histolytica</em>, leishmania, <em>Plasmodium falciparum</em>, <em>Trypanosoma cruzi</em>, <em>Trypanosoma brucei</em>, <em>Toxoplasma gondii</em></td><td></td></tr><tr><td>Helmintic: ascaris, <em>Echinococcus granulosus</em>, Schistosoma, <em>Trichinella spiralis</em>, <em>Wuchereria bancrofti</em></td><td></td></tr></tbody></table></div><div class="table-modal"><table><thead><tr><th>Infectious causes<span aria-hidden="true" style="display: none;"> . </span></th><th>Non-infectious causes<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td>RNA viruses: picornaviruses (coxsackie A + B, echovirus, poliovirus, hepatitis virus), orthomyxovirus (influenza), paramyxoviruses (respiratory syncitial virus, mumps), togaviruses (rubella), flaviviruses (dengue fever, yellow fever)</td><td>Autoimmune diseases: dematomyositis, inflammatory bowel disease, rheumatoid arthritis, sjögren syndrome, systemic lupus erythematodes, Wegener's granulomatosis, giant cell myocarditis</td></tr><tr><td>DNA viruses: adenovirus (A 1, 2 ,3, and 5), erythrovirus [1 (B19V) and 2], herpesviruses (human herpes virus 6 A/B, cytomegalievirus, Epstein-Barr virus, varicella-zoster virus), retrovirus (HIV)</td><td>Drugs: aminophyllin, amphetamine, anthracyclin, catecholamines, chloramphenicol, cocain cyclophosphamid, doxorubicin, 5-fluoruracil, mesylate, methylsergit, phenytoin, trastuzumab, zidovudine</td></tr><tr><td>Bacteria: chlamydia (<em>C. pneumonia</em>/psittacosis) haemophilus influence, legionella, pneumophilia, brucella clostridium, francisella tularensis, neisseria meningitis, mycobacterium (tuberculosis), salmonella, staphylococcus, streptococcus A, S. pneumonia, tularemia, tetanus, syphilis, <em>Vibrio cholera</em></td><td>Hypersensitivity reactions (drugs): azitromycin, benzodiazepines, clozapine, cephalosporins, dapsone, dobutamin, lithium, diuretics, thiazide, methyldopa, mexiletine, Streptomycin, sulfonamides, non-steroidal anti-inflammational drugs, tetanus toxoid, tetracycline, tricyclic antidepressiva</td></tr><tr><td>Spirocheta: <em>Borrelia recurrentis</em>, leptospira, <em>Treponema pallidum</em></td><td>Hypersensitivity reactions (venomes): bee, wasp, black widow spider, scorpion, snakes</td></tr><tr><td>Reckettsia: <em>Coxiella burnetii</em>, <em>R. rickettsii</em>/<em>prowazekii</em></td><td>Systemic diseases: Churg-Strauss syndrome, collagen diseases, sarcoidosis, Kawasaki disease, scleroderma</td></tr><tr><td>Fungi: actinomyces, aspergillus, candida, cryptococcus, histoplasma, nocardia</td><td>Others: heart stroke, hypothermia, transplant rejection, radiation injury</td></tr><tr><td>Protozoa: <em>Entamoeba histolytica</em>, leishmania, <em>Plasmodium falciparum</em>, <em>Trypanosoma cruzi</em>, <em>Trypanosoma brucei</em>, <em>Toxoplasma gondii</em></td><td></td></tr><tr><td>Helmintic: ascaris, <em>Echinococcus granulosus</em>, Schistosoma, <em>Trichinella spiralis</em>, <em>Wuchereria bancrofti</em></td><td></td></tr></tbody></table></div></div></div><div class="table-full-width-wrap"><div class="table-wrap table-wide standard-table"><div class="table-wrap-title" id="EHR165TB1" data-id="EHR165TB1"><span class="label title-label" id="label-17728">Table 1</span><div class="
 graphic-wrap table-open-button-wrap
 "><a class="fig-view-orig at-tableViewLarge openInAnotherWindow btn js-view-large" role="button" target="_blank" href="
 /view-large/6566900" aria-describedby="label-17728"> Open in new tab </a></div><div class="caption caption-id-" id="caption-17728"><p class="chapter-para">Causes of myocarditis</p></div> </div><div class="table-overflow"><table role="table" aria-labelledby="
 label-17728" aria-describedby="
 caption-17728"><thead><tr><th>Infectious causes<span aria-hidden="true" style="display: none;"> . </span></th><th>Non-infectious causes<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td>RNA viruses: picornaviruses (coxsackie A + B, echovirus, poliovirus, hepatitis virus), orthomyxovirus (influenza), paramyxoviruses (respiratory syncitial virus, mumps), togaviruses (rubella), flaviviruses (dengue fever, yellow fever)</td><td>Autoimmune diseases: dematomyositis, inflammatory bowel disease, rheumatoid arthritis, sjögren syndrome, systemic lupus erythematodes, Wegener's granulomatosis, giant cell myocarditis</td></tr><tr><td>DNA viruses: adenovirus (A 1, 2 ,3, and 5), erythrovirus [1 (B19V) and 2], herpesviruses (human herpes virus 6 A/B, cytomegalievirus, Epstein-Barr virus, varicella-zoster virus), retrovirus (HIV)</td><td>Drugs: aminophyllin, amphetamine, anthracyclin, catecholamines, chloramphenicol, cocain cyclophosphamid, doxorubicin, 5-fluoruracil, mesylate, methylsergit, phenytoin, trastuzumab, zidovudine</td></tr><tr><td>Bacteria: chlamydia (<em>C. pneumonia</em>/psittacosis) haemophilus influence, legionella, pneumophilia, brucella clostridium, francisella tularensis, neisseria meningitis, mycobacterium (tuberculosis), salmonella, staphylococcus, streptococcus A, S. pneumonia, tularemia, tetanus, syphilis, <em>Vibrio cholera</em></td><td>Hypersensitivity reactions (drugs): azitromycin, benzodiazepines, clozapine, cephalosporins, dapsone, dobutamin, lithium, diuretics, thiazide, methyldopa, mexiletine, Streptomycin, sulfonamides, non-steroidal anti-inflammational drugs, tetanus toxoid, tetracycline, tricyclic antidepressiva</td></tr><tr><td>Spirocheta: <em>Borrelia recurrentis</em>, leptospira, <em>Treponema pallidum</em></td><td>Hypersensitivity reactions (venomes): bee, wasp, black widow spider, scorpion, snakes</td></tr><tr><td>Reckettsia: <em>Coxiella burnetii</em>, <em>R. rickettsii</em>/<em>prowazekii</em></td><td>Systemic diseases: Churg-Strauss syndrome, collagen diseases, sarcoidosis, Kawasaki disease, scleroderma</td></tr><tr><td>Fungi: actinomyces, aspergillus, candida, cryptococcus, histoplasma, nocardia</td><td>Others: heart stroke, hypothermia, transplant rejection, radiation injury</td></tr><tr><td>Protozoa: <em>Entamoeba histolytica</em>, leishmania, <em>Plasmodium falciparum</em>, <em>Trypanosoma cruzi</em>, <em>Trypanosoma brucei</em>, <em>Toxoplasma gondii</em></td><td></td></tr><tr><td>Helmintic: ascaris, <em>Echinococcus granulosus</em>, Schistosoma, <em>Trichinella spiralis</em>, <em>Wuchereria bancrofti</em></td><td></td></tr></tbody></table></div><div class="table-modal"><table><thead><tr><th>Infectious causes<span aria-hidden="true" style="display: none;"> . </span></th><th>Non-infectious causes<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td>RNA viruses: picornaviruses (coxsackie A + B, echovirus, poliovirus, hepatitis virus), orthomyxovirus (influenza), paramyxoviruses (respiratory syncitial virus, mumps), togaviruses (rubella), flaviviruses (dengue fever, yellow fever)</td><td>Autoimmune diseases: dematomyositis, inflammatory bowel disease, rheumatoid arthritis, sjögren syndrome, systemic lupus erythematodes, Wegener's granulomatosis, giant cell myocarditis</td></tr><tr><td>DNA viruses: adenovirus (A 1, 2 ,3, and 5), erythrovirus [1 (B19V) and 2], herpesviruses (human herpes virus 6 A/B, cytomegalievirus, Epstein-Barr virus, varicella-zoster virus), retrovirus (HIV)</td><td>Drugs: aminophyllin, amphetamine, anthracyclin, catecholamines, chloramphenicol, cocain cyclophosphamid, doxorubicin, 5-fluoruracil, mesylate, methylsergit, phenytoin, trastuzumab, zidovudine</td></tr><tr><td>Bacteria: chlamydia (<em>C. pneumonia</em>/psittacosis) haemophilus influence, legionella, pneumophilia, brucella clostridium, francisella tularensis, neisseria meningitis, mycobacterium (tuberculosis), salmonella, staphylococcus, streptococcus A, S. pneumonia, tularemia, tetanus, syphilis, <em>Vibrio cholera</em></td><td>Hypersensitivity reactions (drugs): azitromycin, benzodiazepines, clozapine, cephalosporins, dapsone, dobutamin, lithium, diuretics, thiazide, methyldopa, mexiletine, Streptomycin, sulfonamides, non-steroidal anti-inflammational drugs, tetanus toxoid, tetracycline, tricyclic antidepressiva</td></tr><tr><td>Spirocheta: <em>Borrelia recurrentis</em>, leptospira, <em>Treponema pallidum</em></td><td>Hypersensitivity reactions (venomes): bee, wasp, black widow spider, scorpion, snakes</td></tr><tr><td>Reckettsia: <em>Coxiella burnetii</em>, <em>R. rickettsii</em>/<em>prowazekii</em></td><td>Systemic diseases: Churg-Strauss syndrome, collagen diseases, sarcoidosis, Kawasaki disease, scleroderma</td></tr><tr><td>Fungi: actinomyces, aspergillus, candida, cryptococcus, histoplasma, nocardia</td><td>Others: heart stroke, hypothermia, transplant rejection, radiation injury</td></tr><tr><td>Protozoa: <em>Entamoeba histolytica</em>, leishmania, <em>Plasmodium falciparum</em>, <em>Trypanosoma cruzi</em>, <em>Trypanosoma brucei</em>, <em>Toxoplasma gondii</em></td><td></td></tr><tr><td>Helmintic: ascaris, <em>Echinococcus granulosus</em>, Schistosoma, <em>Trichinella spiralis</em>, <em>Wuchereria bancrofti</em></td><td></td></tr></tbody></table></div></div></div><p class="chapter-para">Although viral infections can cause serious human diseases, the majority of viral infections are asymptomatic or oligosymptomatic and therefore, such infections are frequently not recognized as possible causes of delayed onset of heart disease.<sup><span class="xrefLink" id="jumplink-EHR165C23"></span><a href="javascript:;" reveal-id="EHR165C23" data-open="EHR165C23" class="link link-ref link-reveal xref-bibr">23</a></sup> In the past, viral myocarditis and chronic viral heart disease have therefore more often been a clinically derived diagnosis of exclusion, rather than a specifically proven diagnosis. Beside the temporary changes of virus epidemics and the geographical differences in the aetiological profiles of viruses, the presence of myocarditic and non-myocarditic virus variants, the enormous variability of clinical symptoms of viral heart disease, which may range from asymptomatic presentation to manifest heart failure, and last but not least the lack of consequent diagnostic efforts for complete virus analysis have hampered an early identification of afflicted patients and thus have prevented the generation of valid epidemiological data.</p> <h2 scrollto-destination=6566902 id="6566902" class="section-title js-splitscreen-section-title" data-legacy-id=s2>Pathogenic mechanisms</h2> <p class="chapter-para">For many viruses, the exact cardiac infection site and the underlying pathogenic mechanisms are unknown. Most information on the pathophysiology of viral heart disease and post-infectious autoimmune myocarditis in both rodent models and humans is known from enteroviral infections such as coxsackievirus B3. Enteroviruses enter the host through the gastrointestinal or respiratory tract, reside in the reticuloendothelial system as an extracardiac reservoir, and attack heart tissue as a secondary target organ. After enterovirus internalization, the negative strand RNA is reversely transcribed into a positive strand for subsequent virus replication.<sup><span class="xrefLink" id="jumplink-EHR165C22"></span><a href="javascript:;" reveal-id="EHR165C22" data-open="EHR165C22" class="link link-ref link-reveal xref-bibr">22</a>,<span class="xrefLink" id="jumplink-EHR165C24"></span><a href="javascript:;" reveal-id="EHR165C24" data-open="EHR165C24" class="link link-ref link-reveal xref-bibr">24</a></sup> A direct virus-related cytolysis of cardiomyocytes is already detected before any inflammatory infiltrate develops and appears to be decisive in fulminant cases of myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C25"></span><a href="javascript:;" reveal-id="EHR165C25" data-open="EHR165C25" class="link link-ref link-reveal xref-bibr">25</a>,<span class="xrefLink" id="jumplink-EHR165C26"></span><a href="javascript:;" reveal-id="EHR165C26" data-open="EHR165C26" class="link link-ref link-reveal xref-bibr">26</a></sup></p><p class="chapter-para">In contrast to enteroviruses, which primarily infect and injure cardiomyocytes, other frequent cardiotropic viruses such as erythroviruses or human herpesvirus 6 A/B infect the vascular endothelial cells (ECs).<sup><span class="xrefLink" id="jumplink-EHR165C27 EHR165C30"></span><a href="javascript:;" reveal-id="EHR165C27 EHR165C30" data-open="EHR165C27 EHR165C30" class="link link-ref link-reveal xref-bibr">27–30</a></sup> Following primary infection in childhood, erythroviruses, including its genotype 1 (parvovirus B19, B19V), may reside asymptomatically in the bone marrow of a vast majority of the adult population. The <em>in vivo</em> tropism of B19V infection is regulated by a number of determinants and persistent infection and replication is mainly restricted to erythroid progenitor cells, but also EC, by the distribution of the primary erythroviral receptor, the P antigen, and reported co-receptors-like integrin α5β1 and the KU80 protein.<sup><span class="xrefLink" id="jumplink-EHR165C31 EHR165C33"></span><a href="javascript:;" reveal-id="EHR165C31 EHR165C33" data-open="EHR165C31 EHR165C33" class="link link-ref link-reveal xref-bibr">31–33</a></sup> With respect to the heart tissue, erythroviruses do not infect cardiomyocytes. In biopsy samples of patients with fulminant myocarditis or sudden onset heart failure, B19V genomes have been localized in EC of venuoles, small arteries, or arterioles.<sup><span class="xrefLink" id="jumplink-EHR165C27"></span><a href="javascript:;" reveal-id="EHR165C27" data-open="EHR165C27" class="link link-ref link-reveal xref-bibr">27</a></sup> In chronic inflammatory cardiomyopathy, B19V infection is predominantly detected in ECs of small capillaries.<sup><span class="xrefLink" id="jumplink-EHR165C28"></span><a href="javascript:;" reveal-id="EHR165C28" data-open="EHR165C28" class="link link-ref link-reveal xref-bibr">28</a>,<span class="xrefLink" id="jumplink-EHR165C29"></span><a href="javascript:;" reveal-id="EHR165C29" data-open="EHR165C29" class="link link-ref link-reveal xref-bibr">29</a></sup></p><p class="chapter-para">Endothelial cell infection is associated with endothelial dysfunction which predicts long-term disease progression in chronic heart failure.<sup><span class="xrefLink" id="jumplink-EHR165C34 EHR165C39"></span><a href="javascript:;" reveal-id="EHR165C34 EHR165C39" data-open="EHR165C34 EHR165C39" class="link link-ref link-reveal xref-bibr">34–39</a></sup> The pathogenetic mechanisms by which B19 exerts endothelial damage are complex and may involve cytotoxicity of the non-structural protein 1, transactivation of interleukin-6 (IL-6), and tumour necrosis factor α, as well as induction of apoptosis as shown <em>in vitro.</em><sup><span class="xrefLink" id="jumplink-EHR165C40 EHR165C45"></span><a href="javascript:;" reveal-id="EHR165C40 EHR165C45" data-open="EHR165C40 EHR165C45" class="link link-ref link-reveal xref-bibr">40–45</a></sup>. Recently, we could show that B19V is released from the bone marrow by infected capillary precursor cells and that interferon-β (IFN-β) improves viability of B19V infected human ECs.<sup><span class="xrefLink" id="jumplink-EHR165C46"></span><a href="javascript:;" reveal-id="EHR165C46" data-open="EHR165C46" class="link link-ref link-reveal xref-bibr">46</a></sup> Since endothelial dysfunction and respective symptoms improved upon IFN-β treatment while both remained unchanged in non-treated patients providing evidence that B19-induced damage of ECs is at least partially mediated via direct virus–cell interaction.<sup><span class="xrefLink" id="jumplink-EHR165C46"></span><a href="javascript:;" reveal-id="EHR165C46" data-open="EHR165C46" class="link link-ref link-reveal xref-bibr">46</a></sup></p><p class="chapter-para">HHV-6 is a lymphotropic virus with tropism mainly for CD4+ and CD8+ T cells, B cells, and natural killer cells. Although HHV-6 is thought of as a lymphotropic virus, it also can infect vascular endothelium.<sup><span class="xrefLink" id="jumplink-EHR165C47"></span><a href="javascript:;" reveal-id="EHR165C47" data-open="EHR165C47" class="link link-ref link-reveal xref-bibr">47</a>,<span class="xrefLink" id="jumplink-EHR165C48"></span><a href="javascript:;" reveal-id="EHR165C48" data-open="EHR165C48" class="link link-ref link-reveal xref-bibr">48</a></sup> Several studies have identified HHV-6-specific DNA in the vascular endothelium <em>in vivo</em>, and suggested EC damage by the virus.<sup><span class="xrefLink" id="jumplink-EHR165C48 EHR165C51"></span><a href="javascript:;" reveal-id="EHR165C48 EHR165C51" data-open="EHR165C48 EHR165C51" class="link link-ref link-reveal xref-bibr">48–51</a></sup> It has been suggested that ECs and cardiac myocytes might be an important reservoir for viral latency and reactivation.<sup><span class="xrefLink" id="jumplink-EHR165C47"></span><a href="javascript:;" reveal-id="EHR165C47" data-open="EHR165C47" class="link link-ref link-reveal xref-bibr">47</a></sup></p><p class="chapter-para">Similar to the other herpes viruses, HHV-6 becomes frequently reactivated by infections or drugs with subacute clinical presentations, especially in acquired or drug-induced immunodeficiencies (e.g. transplant recipients) or in patients with autoimmune disorders. It has been suggested that often HHV-6 rather enhances the pathogenicity of other viruses than being a pathogen itself. In a minority of patients (<1%), HHV-6 is integrated into the chromosome of all nucleated cells resulting in lifelong persistence of HHV-6 which is then passed to 50% of the progenies.</p><p class="chapter-para">Since distinct cardiac target structures are affected by different infectious agents and post-infectious mechanisms, viral myocarditis (viral heart disease) and post-infectious immune myocarditis present with heterogenic clinical phenotypes. If the contractile apparatus (cardiomyocytes) or interstitial cells and matrix structures (e.g. dystrophin) are preferentially involved, ventricular dilatation and systolic heart failure with progression towards post-myocarditic dilated cardiomyopathy (DCM) is directly caused by cytolytic viruses or viral proteases.<sup><span class="xrefLink" id="jumplink-EHR165C52"></span><a href="javascript:;" reveal-id="EHR165C52" data-open="EHR165C52" class="link link-ref link-reveal xref-bibr">52</a></sup> Involvement of vascular tissue (ECs) by other viruses may affect myocardial contractility indirectly, e.g. as a consequence of endothelial dysfunction-associated chronic ischaemia with less often early systolic ventricular dysfunction and possibly slower progression towards systolic heart failure.<sup><span class="xrefLink" id="jumplink-EHR165C36"></span><a href="javascript:;" reveal-id="EHR165C36" data-open="EHR165C36" class="link link-ref link-reveal xref-bibr">36</a>,<span class="xrefLink" id="jumplink-EHR165C46"></span><a href="javascript:;" reveal-id="EHR165C46" data-open="EHR165C46" class="link link-ref link-reveal xref-bibr">46</a>,<span class="xrefLink" id="jumplink-EHR165C53"></span><a href="javascript:;" reveal-id="EHR165C53" data-open="EHR165C53" class="link link-ref link-reveal xref-bibr">53</a>,<span class="xrefLink" id="jumplink-EHR165C54"></span><a href="javascript:;" reveal-id="EHR165C54" data-open="EHR165C54" class="link link-ref link-reveal xref-bibr">54</a></sup> Often patients with EC infection complain for symptoms associated with vasospasm and EC-dysfunction despite normal or nearly normal left ventricular function. The contribution of the virus loads and effects of different virus subtypes are still poorly understood.<sup><span class="xrefLink" id="jumplink-EHR165C55"></span><a href="javascript:;" reveal-id="EHR165C55" data-open="EHR165C55" class="link link-ref link-reveal xref-bibr">55</a></sup> Consequently, distinct viruses with different infection sites in cardiac tissue do not only explain the heterogenic and unpredictable course of viral heart disease with respect to the expression of its phenotype and early or late clinical presentation but also determine indication and response to treatment, or prognosis.</p><p class="chapter-para">Direct cytopathic injury, apoptosis, activation of the innate and adaptive immune system, and cardiac remodelling have all been implicated in the pathogenesis of viral myocarditis. It develops with pathologically distinct phases which time depending determine both clinical presentation and indication for symptomatic or specific treatment strategies (<em>Figure <span class="xrefLink" id="jumplink-EHR165F1"></span><a href="javascript:;" data-modal-source-id="EHR165F1" class="link xref-fig">1</a></em>).<sup><span class="xrefLink" id="jumplink-EHR165C3"></span><a href="javascript:;" reveal-id="EHR165C3" data-open="EHR165C3" class="link link-ref link-reveal xref-bibr">3</a>,<span class="xrefLink" id="jumplink-EHR165C56"></span><a href="javascript:;" reveal-id="EHR165C56" data-open="EHR165C56" class="link link-ref link-reveal xref-bibr">56</a></sup></p> <a id="6566910" scrollto-destination="6566910"></a> <div data-id="ehr165f1" data-content-id="ehr165f1" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16501.gif?Expires=1734529255&Signature=KBHn3UTgTFfQ7IFnPb-Go832vBJSheXrGIEGz-Sax9EnFFD3GgEF6r7gJ-C8P~tQMbRNX~YpVs8v5eUrnVwWhu0Q4U2uwyaDk-NpbTvZ2Fo2~vCQa90SGXW5C~rQB5NXppi0q-7SZBY6bxfJwpnLxrG0OMQtc0FC10I26G2VYw8O-0zALBfdaAEpgz1qduK1VrOyp9dWf-l6IqCPqdqCCnDzNWz6Hz~~z4k2AC3W53P1OcuBbjeKTb-L-c0Jkqbz52EeH7HOpJLIerB7adT7xQvE7xLeVVT4OSDtcgY~QHCUuaMOvO6NtNkEZHUCgZixFMiEa-EVjVvsdK3mnzVTAw__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Distinct phases of myocardial injury in infectious and post-infectious myocarditis. Myocarditis is an inﬂammatory disease of the cardiac muscle caused by myocardial inﬁltration of immunocompetent cells following any kind of cardiac injury. Acute myocarditis is often a result of a viral infection that produces myocardial necrosis and triggers an immune response to eliminate the infectious agent (healed myocarditis and/or dilated cardiomyopathy). Chronic myocardial injury may be caused by post-infectious immune or autoimmune processes [indlammatory cardiomyopathy (DCMi)], be associated with systemic autoimmune diseases or develop by a persisting virus infection (viral heart disease), which, in the long run, are responsible for persistent or progressive ventricular dysfunction, arrhythmias, and cardiac complaints. The disease often presents as an acute form of dilated cardiomyopathy but due to its broad spectrum of presentation the clinical diagnosis is frequently misleading. If the underlying infectious or immune-mediated causes of the disease are carefully defined by clinical and biopsy-based tools, specific immunosuppressive and antiviral treatment options in addition to basic symptomatic therapy may improve prognosis in a number of patients with acute and chronic disease." data-path-from-xml="ehr16501.gif" /><div class="graphic-bottom"><div class="label fig-label" id="label-6566910">Figure 1</div><div class="caption fig-caption"><p class="chapter-para">Distinct phases of myocardial injury in infectious and post-infectious myocarditis. Myocarditis is an inﬂammatory disease of the cardiac muscle caused by myocardial inﬁltration of immunocompetent cells following any kind of cardiac injury. Acute myocarditis is often a result of a viral infection that produces myocardial necrosis and triggers an immune response to eliminate the infectious agent (healed myocarditis and/or dilated cardiomyopathy). Chronic myocardial injury may be caused by post-infectious immune or autoimmune processes [indlammatory cardiomyopathy (DCMi)], be associated with systemic autoimmune diseases or develop by a persisting virus infection (viral heart disease), which, in the long run, are responsible for persistent or progressive ventricular dysfunction, arrhythmias, and cardiac complaints. The disease often presents as an acute form of dilated cardiomyopathy but due to its broad spectrum of presentation the clinical diagnosis is frequently misleading. If the underlying infectious or immune-mediated causes of the disease are carefully defined by clinical and biopsy-based tools, specific immunosuppressive and antiviral treatment options in addition to basic symptomatic therapy may improve prognosis in a number of patients with acute and chronic disease.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-6566910" href="/view-large/figure/6566910/ehr16501.gif" data-path-from-xml="ehr16501.gif" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-6566910" data-section="6566910" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/ehr16501.gif?Expires=1734529255&Signature=W2fX1CpxafGysS5WHOweQVFKEeQvAoiJ3tOfH9t7GVIVJGqKtoNpoXz4DyLswgc3-Ugn06t9EUCZVh1vU7Lh1rMyr94ZvIgPPFVVmOeLRo0GvwGWpPQOEdBz~8K0G8JJjgVcO-u0UBABY~Ft6A5bQwYt7eFerZmYK6I-0ovzz6ZjfyqyWVlsa15sUwb-6umyRXECRqj4Xq-5C7gnl-OmkIBlNRmB6yrSm~fcnQxkAR7P6wnBMCP0OC~DEDI8IFhk0uBNsKqeSOeX2QIQpQOxVmHYchj0hA-MoPTI8CGgkRJPdpPDTHcH3HPKEcs9-1NrKJJuCqEvAJ4CBxVPe3ahow__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=6566910&ar=439730&xsltPath=~/UI/app/XSLT&imagename=&siteId=5375" data-path-from-xml="ehr16501.gif">Download slide</a></div></div></div></div><p class="chapter-para">The early phase of viral myocarditis is initiated by infection of cardiac myocytes, fibroblasts, or ECs through receptor-mediated endocytosis.<sup><span class="xrefLink" id="jumplink-EHR165C57 EHR165C59"></span><a href="javascript:;" reveal-id="EHR165C57 EHR165C59" data-open="EHR165C57 EHR165C59" class="link link-ref link-reveal xref-bibr">57–59</a></sup> Acute myocardial injury can result from either direct virus-mediated lytic processes or are caused by the emerging antiviral immune response (<em>Figure <span class="xrefLink" id="jumplink-EHR165F1"></span><a href="javascript:;" data-modal-source-id="EHR165F1" class="link xref-fig">1</a></em>).<sup><span class="xrefLink" id="jumplink-EHR165C60"></span><a href="javascript:;" reveal-id="EHR165C60" data-open="EHR165C60" class="link link-ref link-reveal xref-bibr">60</a>,<span class="xrefLink" id="jumplink-EHR165C61"></span><a href="javascript:;" reveal-id="EHR165C61" data-open="EHR165C61" class="link link-ref link-reveal xref-bibr">61</a></sup> In fulminant cases of myocarditis, resulting myocyte necrosis may cause a significant loss of contractile tissue, which is accompanied by rapidly developing cardiac failure and early death of the host (early phase). Cytokines released by macrophages and activation of natural killer cells that directly kill virus-infected heart cells through perforin or granzyme-mediated lysis contribute to early myocardial lesions and impaired myocardial function.</p><p class="chapter-para">The activation of antigen-specific immunity mediated by T-cells, B-cells, and antibody production (adaptive immune response) initiates the second phase of virus clearance (<em>Figure <span class="xrefLink" id="jumplink-EHR165F2"></span><a href="javascript:;" data-modal-source-id="EHR165F2" class="link xref-fig">2</a></em>).<sup><span class="xrefLink" id="jumplink-EHR165C62 EHR165C64"></span><a href="javascript:;" reveal-id="EHR165C62 EHR165C64" data-open="EHR165C62 EHR165C64" class="link link-ref link-reveal xref-bibr">62–64</a></sup> The recruitment of leucocytes to sites of infection is crucial to the inflammatory clearance of pathogens. Various molecules may control inflammatory cell trafficking including chemokines, a family of low-molecular-weight proteins involved in adherence of inflammatory cells to activated endothelium and leucocyte chemotaxis (<em>Table <span class="xrefLink" id="jumplink-EHR165TB2"></span><a href="javascript:;" reveal-id="EHR165TB2" data-open="EHR165TB2" class="link link-reveal link-table xref-fig">2</a></em>). Chemokines are important for containment of the infectious agents but may extend tissue injury, if attracted inflammatory cells produce pathological mediators that injure terminally differentiated cardiomyocytes or induce extensive fibrosis (e.g. TGF-β).<sup><span class="xrefLink" id="jumplink-EHR165C65"></span><a href="javascript:;" reveal-id="EHR165C65" data-open="EHR165C65" class="link link-ref link-reveal xref-bibr">65</a></sup></p> <a id="6566913" scrollto-destination="6566913"></a> <div content-id="EHR165TB2" class="table-modal table-full-width-wrap"><div class="table-wrap table-wide standard-table"><div class="table-wrap-title" id="EHR165TB2" data-id="EHR165TB2"><span class="label title-label" id="label-53609">Table 2</span><div class="
 graphic-wrap table-open-button-wrap
 "><a class="fig-view-orig at-tableViewLarge openInAnotherWindow btn js-view-large" role="button" target="_blank" href="
 /view-large/6566913" aria-describedby="label-53609"> Open in new tab </a></div><div class="caption caption-id-" id="caption-53609"><p class="chapter-para">Potential pathogenesis-directed therapies depend on the phase of myocarditis. At all phases, guideline based treatments appropriate to the clinical scenario are indicated</p></div> </div><div class="table-overflow"><table role="table" aria-labelledby="
 label-53609" aria-describedby="
 caption-53609"><thead><tr><th>Phase of disease<span aria-hidden="true" style="display: none;"> . </span></th><th>Proposed mechanism and infectious agents<span aria-hidden="true" style="display: none;"> . </span></th><th>Potential therapy<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td colspan="3">Symptomatic heart failure medication</td></tr><tr><td rowspan="2">Acute myocarditis (early phase)</td><td>Direct cytopathic injury</td><td>Antiviral agents?</td></tr><tr><td>Innate immune system activation (macrophages, NK-cells, and cytokines)</td><td>Antiviral agents? intravenous immune globulin?</td></tr><tr><td rowspan="2">Post-infectious (auto)immunity</td><td rowspan="2">Adaptive immune response (T-cells, B-cells, antibody production)</td><td>Immune modulation</td></tr><tr><td><ul class="bullet"><li><p class="chapter-para">Steroids</p></li><li><p class="chapter-para">Immunoadsorption</p></li><li><p class="chapter-para">Intravenous immune globulin</p></li><li><p class="chapter-para">Muronomab-CD3</p></li></ul></td></tr><tr><td rowspan="11">Chronic viral cardiomyopathy</td><td>Enterovirus</td><td>Interferon-β</td></tr><tr><td>Adenovirus</td><td>Interferon-β</td></tr><tr><td>Erythro-/parvovirus</td><td><ul class="bullet"><li><p class="chapter-para">Intravenous immune globulin (acute infection)</p></li><li><p class="chapter-para">Type I interferons (chronic infection)</p></li></ul></td></tr><tr><td>Human herpesvirus 6</td><td>Val-/Ganciclovir</td></tr><tr><td>Cytomegalovirus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovir</p></li></ul></td></tr><tr><td>Ebstein-Barr virus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovovir</p></li></ul></td></tr><tr><td>Herpes simplex virus</td><td>Aciclovir</td></tr><tr><td>Varicella</td><td>Aciclovir</td></tr><tr><td>Respiratory syntitial virus</td><td>Ribavirin</td></tr><tr><td>Hepatitis C virus</td><td>Pegylated Interferon-α + ribavirin</td></tr><tr><td>HIV</td><td>Anti-retrovirals</td></tr></tbody></table></div><div class="table-modal"><table><thead><tr><th>Phase of disease<span aria-hidden="true" style="display: none;"> . </span></th><th>Proposed mechanism and infectious agents<span aria-hidden="true" style="display: none;"> . </span></th><th>Potential therapy<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td colspan="3">Symptomatic heart failure medication</td></tr><tr><td rowspan="2">Acute myocarditis (early phase)</td><td>Direct cytopathic injury</td><td>Antiviral agents?</td></tr><tr><td>Innate immune system activation (macrophages, NK-cells, and cytokines)</td><td>Antiviral agents? intravenous immune globulin?</td></tr><tr><td rowspan="2">Post-infectious (auto)immunity</td><td rowspan="2">Adaptive immune response (T-cells, B-cells, antibody production)</td><td>Immune modulation</td></tr><tr><td><ul class="bullet"><li><p class="chapter-para">Steroids</p></li><li><p class="chapter-para">Immunoadsorption</p></li><li><p class="chapter-para">Intravenous immune globulin</p></li><li><p class="chapter-para">Muronomab-CD3</p></li></ul></td></tr><tr><td rowspan="11">Chronic viral cardiomyopathy</td><td>Enterovirus</td><td>Interferon-β</td></tr><tr><td>Adenovirus</td><td>Interferon-β</td></tr><tr><td>Erythro-/parvovirus</td><td><ul class="bullet"><li><p class="chapter-para">Intravenous immune globulin (acute infection)</p></li><li><p class="chapter-para">Type I interferons (chronic infection)</p></li></ul></td></tr><tr><td>Human herpesvirus 6</td><td>Val-/Ganciclovir</td></tr><tr><td>Cytomegalovirus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovir</p></li></ul></td></tr><tr><td>Ebstein-Barr virus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovovir</p></li></ul></td></tr><tr><td>Herpes simplex virus</td><td>Aciclovir</td></tr><tr><td>Varicella</td><td>Aciclovir</td></tr><tr><td>Respiratory syntitial virus</td><td>Ribavirin</td></tr><tr><td>Hepatitis C virus</td><td>Pegylated Interferon-α + ribavirin</td></tr><tr><td>HIV</td><td>Anti-retrovirals</td></tr></tbody></table></div></div></div><div class="table-full-width-wrap"><div class="table-wrap table-wide standard-table"><div class="table-wrap-title" id="EHR165TB2" data-id="EHR165TB2"><span class="label title-label" id="label-53609">Table 2</span><div class="
 graphic-wrap table-open-button-wrap
 "><a class="fig-view-orig at-tableViewLarge openInAnotherWindow btn js-view-large" role="button" target="_blank" href="
 /view-large/6566913" aria-describedby="label-53609"> Open in new tab </a></div><div class="caption caption-id-" id="caption-53609"><p class="chapter-para">Potential pathogenesis-directed therapies depend on the phase of myocarditis. At all phases, guideline based treatments appropriate to the clinical scenario are indicated</p></div> </div><div class="table-overflow"><table role="table" aria-labelledby="
 label-53609" aria-describedby="
 caption-53609"><thead><tr><th>Phase of disease<span aria-hidden="true" style="display: none;"> . </span></th><th>Proposed mechanism and infectious agents<span aria-hidden="true" style="display: none;"> . </span></th><th>Potential therapy<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td colspan="3">Symptomatic heart failure medication</td></tr><tr><td rowspan="2">Acute myocarditis (early phase)</td><td>Direct cytopathic injury</td><td>Antiviral agents?</td></tr><tr><td>Innate immune system activation (macrophages, NK-cells, and cytokines)</td><td>Antiviral agents? intravenous immune globulin?</td></tr><tr><td rowspan="2">Post-infectious (auto)immunity</td><td rowspan="2">Adaptive immune response (T-cells, B-cells, antibody production)</td><td>Immune modulation</td></tr><tr><td><ul class="bullet"><li><p class="chapter-para">Steroids</p></li><li><p class="chapter-para">Immunoadsorption</p></li><li><p class="chapter-para">Intravenous immune globulin</p></li><li><p class="chapter-para">Muronomab-CD3</p></li></ul></td></tr><tr><td rowspan="11">Chronic viral cardiomyopathy</td><td>Enterovirus</td><td>Interferon-β</td></tr><tr><td>Adenovirus</td><td>Interferon-β</td></tr><tr><td>Erythro-/parvovirus</td><td><ul class="bullet"><li><p class="chapter-para">Intravenous immune globulin (acute infection)</p></li><li><p class="chapter-para">Type I interferons (chronic infection)</p></li></ul></td></tr><tr><td>Human herpesvirus 6</td><td>Val-/Ganciclovir</td></tr><tr><td>Cytomegalovirus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovir</p></li></ul></td></tr><tr><td>Ebstein-Barr virus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovovir</p></li></ul></td></tr><tr><td>Herpes simplex virus</td><td>Aciclovir</td></tr><tr><td>Varicella</td><td>Aciclovir</td></tr><tr><td>Respiratory syntitial virus</td><td>Ribavirin</td></tr><tr><td>Hepatitis C virus</td><td>Pegylated Interferon-α + ribavirin</td></tr><tr><td>HIV</td><td>Anti-retrovirals</td></tr></tbody></table></div><div class="table-modal"><table><thead><tr><th>Phase of disease<span aria-hidden="true" style="display: none;"> . </span></th><th>Proposed mechanism and infectious agents<span aria-hidden="true" style="display: none;"> . </span></th><th>Potential therapy<span aria-hidden="true" style="display: none;"> . </span></th></tr></thead><tbody><tr><td colspan="3">Symptomatic heart failure medication</td></tr><tr><td rowspan="2">Acute myocarditis (early phase)</td><td>Direct cytopathic injury</td><td>Antiviral agents?</td></tr><tr><td>Innate immune system activation (macrophages, NK-cells, and cytokines)</td><td>Antiviral agents? intravenous immune globulin?</td></tr><tr><td rowspan="2">Post-infectious (auto)immunity</td><td rowspan="2">Adaptive immune response (T-cells, B-cells, antibody production)</td><td>Immune modulation</td></tr><tr><td><ul class="bullet"><li><p class="chapter-para">Steroids</p></li><li><p class="chapter-para">Immunoadsorption</p></li><li><p class="chapter-para">Intravenous immune globulin</p></li><li><p class="chapter-para">Muronomab-CD3</p></li></ul></td></tr><tr><td rowspan="11">Chronic viral cardiomyopathy</td><td>Enterovirus</td><td>Interferon-β</td></tr><tr><td>Adenovirus</td><td>Interferon-β</td></tr><tr><td>Erythro-/parvovirus</td><td><ul class="bullet"><li><p class="chapter-para">Intravenous immune globulin (acute infection)</p></li><li><p class="chapter-para">Type I interferons (chronic infection)</p></li></ul></td></tr><tr><td>Human herpesvirus 6</td><td>Val-/Ganciclovir</td></tr><tr><td>Cytomegalovirus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovir</p></li></ul></td></tr><tr><td>Ebstein-Barr virus</td><td><ul class="bullet"><li><p class="chapter-para">Val-/ganciclovir</p></li><li><p class="chapter-para">Foscanet</p></li><li><p class="chapter-para">Cidovovir</p></li></ul></td></tr><tr><td>Herpes simplex virus</td><td>Aciclovir</td></tr><tr><td>Varicella</td><td>Aciclovir</td></tr><tr><td>Respiratory syntitial virus</td><td>Ribavirin</td></tr><tr><td>Hepatitis C virus</td><td>Pegylated Interferon-α + ribavirin</td></tr><tr><td>HIV</td><td>Anti-retrovirals</td></tr></tbody></table></div></div></div> <a id="6566914" scrollto-destination="6566914"></a> <div data-id="ehr165f2" data-content-id="ehr165f2" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16502.gif?Expires=1734529255&Signature=Z4Oqc1LVXnJYO1D0DgGCKiWuqBydB-L9XMSeL8Foyb~AbUMQUJYDeBhTLYhLwGEs7c5lB7BsHXwcE~DoVNpFE2N-AL1JxBx2vtKMrKjfQZJ8o~aWyxVEdQxHXtoWI7wYOJuKhe7aI5gSXcZSL~MCG0aypywhY8CqqvUWssjhGKsdwN2df4Zi4~Dns1dCqvoYWvsdTkjEDhQN64NgRn1wcCMunvNIAGCFYbIp-6LoJziAlCb4j36X6tUp5v0KpNje2DGDyMlDY9~6u4xKy0QOQwZDmJAp8ClYtL5TwnSDJflBrN6T6yUyRLK-YAtrMSGpqRw6laMCyXuX7-J4rswOyQ__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Infection of cardiac endothelial cells or cardiac myocytes by virus causes direct cellular damage and subsequently an innate and adaptive immune response, all of which contribute to cardiomyopathy. Cardiomyopathy from viral injury and the subsequent immune reaction can include diastolic as well as systolic dysfunction." data-path-from-xml="ehr16502.gif" /><div class="graphic-bottom"><div class="label fig-label" id="label-6566914">Figure 2</div><div class="caption fig-caption"><p class="chapter-para">Infection of cardiac endothelial cells or cardiac myocytes by virus causes direct cellular damage and subsequently an innate and adaptive immune response, all of which contribute to cardiomyopathy. Cardiomyopathy from viral injury and the subsequent immune reaction can include diastolic as well as systolic dysfunction.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-6566914" href="/view-large/figure/6566914/ehr16502.gif" data-path-from-xml="ehr16502.gif" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-6566914" data-section="6566914" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/ehr16502.gif?Expires=1734529255&Signature=ZAdzRQB0vBEbnow4GTDWpxfJaVvBvD3fYZ9j1GFqjLa6RGxBthH8gq~mQArlE5oLD4xD0oF739ggYX2rDH8lAFKQCIg28vs-0zJd~koSwzLa6l-E3LwiAc8ncXvIbZxQCV9rT90A1jjfXgbTFtLx8C8hXDK-L9lxnM7u4Be7OdxqSxndKz4Cog-bwSprItYt~BRnhRdAIEafHk1YvNqtqJ8KKjjIygCn6z9kqw3c779EoFmG4SjOcwnYsmIIePuaApyFNVse5UZ1U9ygeOUvyQQxnjarc~rV2WVXWK1NTxpmX2r-zhEb8X09ZzvwqdqBqtN3WVzOmbnShq1ZKkJ~Lg__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=6566914&ar=439730&xsltPath=~/UI/app/XSLT&imagename=&siteId=5375" data-path-from-xml="ehr16502.gif">Download slide</a></div></div></div></div><p class="chapter-para">T-regulatory cells are also important in inhibiting the pathogenesis of acute viral myocarditis and subsequent dilated cardiomyopathy. Adoptive transfer of T-regulatory cells protects mice from coxsackievirus B3 (CVB3)-induced myocarditis through the transforming growth factor β-coxsackie-adenovirus receptor pathway and thus suppresses the immune response to cardiac tissue.<sup><span class="xrefLink" id="jumplink-EHR165C66"></span><a href="javascript:;" reveal-id="EHR165C66" data-open="EHR165C66" class="link link-ref link-reveal xref-bibr">66</a></sup> Coxsackievirus B3 causes severe myocarditis in BALB/c mice. BALB/c mice receiving CD4(+) CD25(+) T regulatory cells from γδ(+) T-cell-depleted donors developed significantly less myocarditis and CD4(+) Th1 cell responses compared with mice receiving equal numbers of CD4(+) CD25(+) cells from infected γδ (+) T-cell-sufficient animals. This study showed that γδ (+) cells promote CD4(+) IFN-γ(+) acute and memory responses by limiting FoxP3(+) T regulatory cell activation.<sup><span class="xrefLink" id="jumplink-EHR165C67"></span><a href="javascript:;" reveal-id="EHR165C67" data-open="EHR165C67" class="link link-ref link-reveal xref-bibr">67</a></sup> Finally, male BALB/c mice infected with CVB3 develop more severe acute inflammation in the heart compared with females due to fewer T regulatory cells and Tim-3(+) M2 macrophages.<sup><span class="xrefLink" id="jumplink-EHR165C68"></span><a href="javascript:;" reveal-id="EHR165C68" data-open="EHR165C68" class="link link-ref link-reveal xref-bibr">68</a></sup></p><p class="chapter-para">Negative immune modulation, an important property of an intact immune system to prevent excessive tissue damage by an overwhelming immune response, normally occurs rapidly after successful elimination of the infectious pathogens. Under certain circumstances, chronic immune stimulation and autoimmunity may result from incompletely cleared virus infection or in response to the virus- and immune-mediated chronic tissue damage, respectively. Both cellular and humeral inflammatory processes may contribute to the progression of chronic myocardial injury.<sup><span class="xrefLink" id="jumplink-EHR165C69"></span><a href="javascript:;" reveal-id="EHR165C69" data-open="EHR165C69" class="link link-ref link-reveal xref-bibr">69</a></sup> The underlying pathological processes are not well understood but in chronic inflammatory cardiomyopathy, subgroups of patients may benefit from immunosuppression.</p><p class="chapter-para">If viral infection and autoimmune processes have resolved, the magnitude of the remaining tissue damage determines the further course of the disease.<sup><span class="xrefLink" id="jumplink-EHR165C70"></span><a href="javascript:;" reveal-id="EHR165C70" data-open="EHR165C70" class="link link-ref link-reveal xref-bibr">70</a></sup> This late phase of post-infectious disease is distinguished by cardiac remodelling, progressive dilitation, and chronic heart failure. Aetiology-specific treatment is probably not useful but only standard heart failure medication and/or devices may prevent or delay progression and improve prognosis.</p><p class="chapter-para">Genetic predisposition is a likely factor in some cases of myocarditis, although direct evidence in human disease is lacking. In murine models of myocarditis, genetic predisposition to Th1, Th2, and Th17 cytokine responses influence the severity and time course of viral infection (reviewed in Rose 2009).<sup><span class="xrefLink" id="jumplink-EHR165C71"></span><a href="javascript:;" reveal-id="EHR165C71" data-open="EHR165C71" class="link link-ref link-reveal xref-bibr">71</a></sup> Similarly, truncations in the 5′ untranslated region of the Coxsackie B virus genome can lower viral replication rate and lead to chronic infection.<sup><span class="xrefLink" id="jumplink-EHR165C72"></span><a href="javascript:;" reveal-id="EHR165C72" data-open="EHR165C72" class="link link-ref link-reveal xref-bibr">72</a></sup> Few genomic studies in human disease have been performed in part due to relatively small patient cohorts and lack of large multi-centre biobanks linked to well-characterized clinical phenotypes with outcome data.</p><p class="chapter-para">Autoimmune myocarditis, exemplified by giant cell myocarditis, usually occurs without an identified trigger such as a viral infection; although vial infection can amplify naturally occurring autoantibodies and autoreactive T cells. The time course of cytokine and chemokine expression following experimental autoimmune myocarditis in the Lewis rat is similar to the pattern observed in models of severe enteroviral myocarditis (<em>Figure <span class="xrefLink" id="jumplink-EHR165F3"></span><a href="javascript:;" data-modal-source-id="EHR165F3" class="link xref-fig">3</a></em>)<sup><span class="xrefLink" id="jumplink-EHR165C73"></span><a href="javascript:;" reveal-id="EHR165C73" data-open="EHR165C73" class="link link-ref link-reveal xref-bibr">73</a></sup> The early rise in pro-inflammatory cytokines such as Il-2 and IFN-γ, is followed by regulatory cytokines such as IL-10 and profibrotic cytokines like TGF-β1.<sup><span class="xrefLink" id="jumplink-EHR165C65"></span><a href="javascript:;" reveal-id="EHR165C65" data-open="EHR165C65" class="link link-ref link-reveal xref-bibr">65</a>,<span class="xrefLink" id="jumplink-EHR165C74 EHR165C76"></span><a href="javascript:;" reveal-id="EHR165C74 EHR165C76" data-open="EHR165C74 EHR165C76" class="link link-ref link-reveal xref-bibr">74–76</a></sup> However, in other models of autoimmune and viral myocarditis gender, hormone milieu, and the nature of the initial innate immune response impact the severity and time course of subsequent inflammation and cardiomyopathy.<sup><span class="xrefLink" id="jumplink-EHR165C77"></span><a href="javascript:;" reveal-id="EHR165C77" data-open="EHR165C77" class="link link-ref link-reveal xref-bibr">77</a>,<span class="xrefLink" id="jumplink-EHR165C78"></span><a href="javascript:;" reveal-id="EHR165C78" data-open="EHR165C78" class="link link-ref link-reveal xref-bibr">78</a></sup> In naïve BABL/c mice organ-specific, IL-17-mediated autoimmunity and heart failure is induced by self-antigen loaded activated dendritic cells (DCs) that prime MYHC-α-specific CD4 T-cells if DCs are activated through toll-like receptors and CD40 costimulation.<sup><span class="xrefLink" id="jumplink-EHR165C79"></span><a href="javascript:;" reveal-id="EHR165C79" data-open="EHR165C79" class="link link-ref link-reveal xref-bibr">79</a>,<span class="xrefLink" id="jumplink-EHR165C80"></span><a href="javascript:;" reveal-id="EHR165C80" data-open="EHR165C80" class="link link-ref link-reveal xref-bibr">80</a></sup> In such a model, suppression of activated autoreactive Th17-cells by IFN-γ-producing monocytes limits cardiac inflammation and prevents further tissue injury.<sup><span class="xrefLink" id="jumplink-EHR165C81"></span><a href="javascript:;" reveal-id="EHR165C81" data-open="EHR165C81" class="link link-ref link-reveal xref-bibr">81</a></sup></p> <a id="6566920" scrollto-destination="6566920"></a> <div data-id="ehr165f3" data-content-id="ehr165f3" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/m_ehr16503.gif?Expires=1734529255&Signature=nsbks7h4F-P3Ppx2vO6CUDS~VxqJZ4rUI1VeRod59cUQCE-Vasly88LX7NqybrewsTe3s1-MLrQh-7IqujAIZDUfDBYdR~xwIAg-VZtBAD-GFSacthuziy1xVmpYGY7pNis9mB-RG5BpIkaEbzGjUDdC4qcnW-83A-6x3zu3qVEe1ZM3yKk89D6w~qicJB7-s0y7Z95qzFRax~6qsvBnCGA-Y5eIzjiXgFoWoSMVMuV5q9Yjr6Khoz4xSLcKwnpMD9KaA2xEz7YULkIvlwjk8~jhPDurJobQHeaKKQaQ--iU9MpK11DFZrDZ1n404Y9zHhmjsVDEx~ADDfY3Gs3Pyw__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Adapted from Kodama M. et al. Animal Models of Autoimmune Myocarditis, in Cooper, LT, ed, Myocarditis from Bench to Bedside. Humana Press, Towtowa, NJ 2003." data-path-from-xml="ehr16503.gif" /><div class="graphic-bottom"><div class="label fig-label" id="label-6566920">Figure 3</div><div class="caption fig-caption"><p class="chapter-para">Adapted from Kodama M. et al. Animal Models of Autoimmune Myocarditis, in Cooper, LT, ed, Myocarditis from Bench to Bedside. Humana Press, Towtowa, NJ 2003.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-6566920" href="/view-large/figure/6566920/ehr16503.gif" data-path-from-xml="ehr16503.gif" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-6566920" data-section="6566920" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/eurheartj/32/21/10.1093/eurheartj/ehr165/2/ehr16503.gif?Expires=1734529255&Signature=r2xUf5O5EWhMhCRP-wZGTiW2PP3UASjfuF5UvAPD-w71BjjJ2ydR66c-ctpKnlSfndi2BrhNSZ~tKU~KO9m67HDzO40772EJO4Npb-YyBbQVq1CL3B9IOuGbGqfONHgNLZQZQYzLkLi46qiTNGvWUmddCFLOgY6KXKs7d0o729SOxXmgTvlIic5DL626F51Mep3NxkHAS9g5ggG4ix711YPDIoKTD-Mto43mbKWOws2iSo4H6xXMVJolJy5dGdIluxiERJ6LWX8u2QxUZk9npMx9cWVE7ol9mS7ZKuq05cxRONTfNPq7CMHhkvZ5TuYuN3BTbvyYQ2uyDmCV4isvHQ__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=6566920&ar=439730&xsltPath=~/UI/app/XSLT&imagename=&siteId=5375" data-path-from-xml="ehr16503.gif">Download slide</a></div></div></div></div><div id="" class="boxed-text boxed-matter no-caption"><p class="chapter-para"><em>Select knowledge gaps and opportunities in the pathogenesis of myocarditis</em></p><p class="chapter-para">• The heterogeneity of clinical presentations and incomplete understanding of human immunopathology are obstacles to current investigation.</p><p class="chapter-para">• The major long-term consequence of myocarditis is chronic dilated cardiomyopathy, but the pathways that lead to myocardial fibrosis are poorly understood.</p><p class="chapter-para">• Investigation of the pathways that lead to fibrosis and DCM after viral injury requires bidirectional collaboration between investigators with small animal models that recapitulate late cardiac fibrosis and clinicians who take a multi-centre, programmatic approach to patient care.</p><p class="chapter-para">• The genetic factors contributing to human myocarditis are poorly understood. Advances in the genetics of myocarditis will require multi-centre, pathogen-specific registries with linked biobanks, core facilities with next generation whole genome sequencing and candidate driven transcriptomic and metabolomic studies.</p></div> <h2 scrollto-destination=6566922 id="6566922" class="section-title js-splitscreen-section-title" data-legacy-id=s3>Diagnosis and prognosis</h2> <p class="chapter-para">The clinical presentation of acute myocarditis ranges broadly from subclinical disease to fulminant heart failure, and chest pain, palpitations, and syncope are not uncommon. Young children often have a more fulminant presentation than adults.<sup><span class="xrefLink" id="jumplink-EHR165C82"></span><a href="javascript:;" reveal-id="EHR165C82" data-open="EHR165C82" class="link link-ref link-reveal xref-bibr">82</a></sup> Men with presumed viral myocarditis may have more severe damage than women.<sup><span class="xrefLink" id="jumplink-EHR165C83"></span><a href="javascript:;" reveal-id="EHR165C83" data-open="EHR165C83" class="link link-ref link-reveal xref-bibr">83</a></sup> A viral prodrome including fever and respiratory or gastrointestinal symptoms frequently precedes the onset of myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C84"></span><a href="javascript:;" reveal-id="EHR165C84" data-open="EHR165C84" class="link link-ref link-reveal xref-bibr">84</a></sup> Chest pain in acute myocarditis may resemble angina with ischaemic electrocardiographic changes or be more typical for pericarditis, when both the epicardium and adjacent pericardium are inflamed. In a representative sample of the adult patients screened in the European Study of the Epidemiology and Treatment of inflammatory Heart Disease, 72% had dyspnoea, 32% had chest pain, and 18% had arrhythmias.<sup><span class="xrefLink" id="jumplink-EHR165C85"></span><a href="javascript:;" reveal-id="EHR165C85" data-open="EHR165C85" class="link link-ref link-reveal xref-bibr">85</a></sup></p><p class="chapter-para">The sensitivity of cardiac biomarkers of myocardial injury varies depending on the time from symptom onset to testing and the cut-off values used. For example, in acute paediatric myocarditis, the sensitivity of specificity of Troponin T (TnT) were 75 and 75% when the cut-off was set at 0.026 ng/mL and 63 and 89% with a cut-off value of 0.071 ng/mL.<sup><span class="xrefLink" id="jumplink-EHR165C86"></span><a href="javascript:;" reveal-id="EHR165C86" data-open="EHR165C86" class="link link-ref link-reveal xref-bibr">86</a></sup> Elevations of Troponin I (TnI) in patients with myocarditis were significantly correlated with ≤1-month duration of heart failure symptoms.<sup><span class="xrefLink" id="jumplink-EHR165C87"></span><a href="javascript:;" reveal-id="EHR165C87" data-open="EHR165C87" class="link link-ref link-reveal xref-bibr">87</a></sup> Troponin I or TnT are more commonly elevated than creatinine kinase MB in both adults and children with acute myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C87 EHR165C89"></span><a href="javascript:;" reveal-id="EHR165C87 EHR165C89" data-open="EHR165C87 EHR165C89" class="link link-ref link-reveal xref-bibr">87–89</a></sup> Non-specific serum makers of inflammation, including erythrocyte sedimentation rate, C-reactive protein, and leucocyte count may be elevated.</p><p class="chapter-para">The most common electrocardiogram (ECG) findings are non-specific T-wave changes.<sup><span class="xrefLink" id="jumplink-EHR165C90"></span><a href="javascript:;" reveal-id="EHR165C90" data-open="EHR165C90" class="link link-ref link-reveal xref-bibr">90</a></sup> Occasionally, the ECG changes may mimic acute myocardial infarction or pericarditis with ST segment elevation, ST segment depression, PR segment depression, and pathological Q-waves.<sup><span class="xrefLink" id="jumplink-EHR165C91"></span><a href="javascript:;" reveal-id="EHR165C91" data-open="EHR165C91" class="link link-ref link-reveal xref-bibr">91</a>,<span class="xrefLink" id="jumplink-EHR165C92"></span><a href="javascript:;" reveal-id="EHR165C92" data-open="EHR165C92" class="link link-ref link-reveal xref-bibr">92</a></sup> Tachyarrhythmias are often non-sustained and rarely cause haemodynamic compromise in adult viral myocarditis. The prognostic significance and optimal management of non-sustained ventricular tachycardia in the setting of acute myocarditis are not known. However, Q-waves and a widened QRS complex, including left bundle branch block, are associated with higher rates of death or cardiac transplantation.<sup><span class="xrefLink" id="jumplink-EHR165C90"></span><a href="javascript:;" reveal-id="EHR165C90" data-open="EHR165C90" class="link link-ref link-reveal xref-bibr">90</a>,<span class="xrefLink" id="jumplink-EHR165C93 EHR165C95"></span><a href="javascript:;" reveal-id="EHR165C93 EHR165C95" data-open="EHR165C93 EHR165C95" class="link link-ref link-reveal xref-bibr">93–95</a></sup></p><p class="chapter-para">Echocardiography is useful to exclude other causes of heart failure and identify ventricular thrombi. There are no specific echocardiographic features of myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C96"></span><a href="javascript:;" reveal-id="EHR165C96" data-open="EHR165C96" class="link link-ref link-reveal xref-bibr">96</a>,<span class="xrefLink" id="jumplink-EHR165C97"></span><a href="javascript:;" reveal-id="EHR165C97" data-open="EHR165C97" class="link link-ref link-reveal xref-bibr">97</a></sup> Indeed, segmental or global wall motion abnormalities can mimic myocardial infarction.<sup><span class="xrefLink" id="jumplink-EHR165C98"></span><a href="javascript:;" reveal-id="EHR165C98" data-open="EHR165C98" class="link link-ref link-reveal xref-bibr">98</a></sup> Patients with fulminant myocarditis tend to present with more normal cardiac chamber dimensions and thickened walls, compared with patients with less acute myocarditis who have greater left ventricular dilation and normal wall thickness.<sup><span class="xrefLink" id="jumplink-EHR165C99"></span><a href="javascript:;" reveal-id="EHR165C99" data-open="EHR165C99" class="link link-ref link-reveal xref-bibr">99</a></sup> Right ventricular dysfunction is an uncommon but important predictor of death or cardiac transplantation.<sup><span class="xrefLink" id="jumplink-EHR165C100"></span><a href="javascript:;" reveal-id="EHR165C100" data-open="EHR165C100" class="link link-ref link-reveal xref-bibr">100</a></sup> Newer imaging techniques including strain echocardiography may have better specificity and specificity for myocarditis.</p><p class="chapter-para">Cardiovascular magnetic resonance (CMR) in suspected myocarditis can localize and quantitate tissue injury, including oedema, hyperaemia, and fibrosis.<sup><span class="xrefLink" id="jumplink-EHR165C101"></span><a href="javascript:;" reveal-id="EHR165C101" data-open="EHR165C101" class="link link-ref link-reveal xref-bibr">101</a></sup> In a recent series of 82 patients with myocarditis all of whom had biopsy-proven disease, CMR alone made the correct diagnosis in 80% (66 out of 82) cases.<sup><span class="xrefLink" id="jumplink-EHR165C102"></span><a href="javascript:;" reveal-id="EHR165C102" data-open="EHR165C102" class="link link-ref link-reveal xref-bibr">102</a></sup> However, both T2- and T1-weighted imaging are needed to achieve optimal sensitivity and specificity, and in contrast to older reports, CMR abnormalities do not correlate closely with endomyocardial biopsy (EMB) evidence of myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C39"></span><a href="javascript:;" reveal-id="EHR165C39" data-open="EHR165C39" class="link link-ref link-reveal xref-bibr">39</a></sup> When two or more of the three ‘Lake Louise' criteria are positive, myocardial inflammation can be predicted with a diagnostic accuracy of 78%; if only delayed, post-gadolinium enhancement imaging is performed, the diagnostic accuracy drops to 68%.<sup><span class="xrefLink" id="jumplink-EHR165C101"></span><a href="javascript:;" reveal-id="EHR165C101" data-open="EHR165C101" class="link link-ref link-reveal xref-bibr">101</a></sup> Prospective clinical studies of the prognostic value of CMR are needed to identify whether tissue characterization adds to the management or outcome of patients with myocarditis.</p><p class="chapter-para">Confirmation of myocarditis still requires histological or immunohistological evidence of inflammation in heart tissue. Endomyocardial biopsy can be performed with a very low major complication rate when performed by highly experienced operators.<sup><span class="xrefLink" id="jumplink-EHR165C103"></span><a href="javascript:;" reveal-id="EHR165C103" data-open="EHR165C103" class="link link-ref link-reveal xref-bibr">103</a></sup> In experienced hands, left ventricular biopsy is as safe as right ventricular biopsy.<sup><span class="xrefLink" id="jumplink-EHR165C39"></span><a href="javascript:;" reveal-id="EHR165C39" data-open="EHR165C39" class="link link-ref link-reveal xref-bibr">39</a></sup> An AHA/ACCF/ESC joint scientific statement recommended that EMB should be performed (Class I indication) in patients with heart failure and (i) a normal sized or dilated left ventricle, <2 weeks of symptoms, and haemodynamic compromise and also in (ii) patents with a dilated ventricle, 2 weeks to 3 months of symptoms, new ventricular arrhythmias or Mobitz type II second degree or third degree heart block, or who fail to respond to usual care within 1–2 weeks.<sup><span class="xrefLink" id="jumplink-EHR165C104"></span><a href="javascript:;" reveal-id="EHR165C104" data-open="EHR165C104" class="link link-ref link-reveal xref-bibr">104</a></sup> More recently, EMB-based criteria (inflammation present by immunohistology and viral genomes absent by polymerase chain reaction) have been used to define a cohort of patients with chronic DCM who respond to immunosuppression.<sup><span class="xrefLink" id="jumplink-EHR165C105"></span><a href="javascript:;" reveal-id="EHR165C105" data-open="EHR165C105" class="link link-ref link-reveal xref-bibr">105</a></sup> In clinical practice, EMB should be used in those scenarios in which the incremental prognostic and therapeutic information gained from biopsy outweighs the risk and cost. This will vary by medical centre, depending on availability of necessary facilities and expertise.</p><div id="" class="boxed-text boxed-matter no-caption"><p class="chapter-para"><em>Select knowledge gaps and opportunities in the diagnosis and prognosis of myocarditis</em></p><p class="chapter-para">• The incidence and prevalence of myocarditis are unknown. There is an immediate need for inexpensive, sensitive, and specific diagnostic tests that can be used in population-based studies in regions without access to advanced imaging or cardiac catheterization laboratories.</p><p class="chapter-para">• Gender issues: the protective effect of estrogens and the role of viral myocarditis in peripartum cardiomyopathy are incompletely understood.</p><p class="chapter-para">• Paediatric cases: the optimal strategy for diagnosing myocarditis in children is controversial and based largely on expert opinion.</p><p class="chapter-para">• Molecular inflammatory markers in peripheral blood combined with newer echocardiographic and CMR imaging techniques and EMB may lead to more accurate diagnosis and aetiology-specific treatments.</p></div> <h2 scrollto-destination=6566930 id="6566930" class="section-title js-splitscreen-section-title" data-legacy-id=s4>Treatment</h2> <p class="chapter-para">Cardiomyocytes can be destroyed by direct virus damage, the antiviral immune response, or a truly autoimmune injury. Since adult cardiomyocytes rarely regenerate, recovery of myocardial function depends on the residual myocardial tissue. The treatment response of acute and chronic myocarditis therefore depends on the specific causes of the disease, severity of irreversible tissue alterations at the onset of treatment and consequently on the potential of the myocardium to compensate for such processes. If the pre-treatment damage is severe, aetiology-specific treatment options at best can halt rapid progression of the disease but will not achieve significant improvement in ventricular function.</p> <h3 scrollto-destination=6566932 id="6566932" class="section-title js-splitscreen-section-title" data-legacy-id=s4a>Treatment for heart failure</h3> <p class="chapter-para">The mainstay of treatment for myocarditis presenting as dilated cardiomyopathy is an optimal heart failure medical regimen. If the left ventricular ejection fraction (LVEF) is <40%, we recommend that an angiotensin-converting enzyme-inhibitor/angiotensin receptor blocker and/or a β-adrenergic blocking agent be used according to the current AHA/ACCF and ESC guidelines for the management of heart failure.<sup><span class="xrefLink" id="jumplink-EHR165C106 EHR165C108"></span><a href="javascript:;" reveal-id="EHR165C106 EHR165C108" data-open="EHR165C106 EHR165C108" class="link link-ref link-reveal xref-bibr">106–108</a></sup> Supporting this strategy are experimental studies that show captopril and candesartan improve myocarditis in murine myocarditis models.<sup><span class="xrefLink" id="jumplink-EHR165C109"></span><a href="javascript:;" reveal-id="EHR165C109" data-open="EHR165C109" class="link link-ref link-reveal xref-bibr">109</a>,<span class="xrefLink" id="jumplink-EHR165C110"></span><a href="javascript:;" reveal-id="EHR165C110" data-open="EHR165C110" class="link link-ref link-reveal xref-bibr">110</a></sup> Non-steroidal anti-inflammatory agents such as indomethacin should be considered for patients with a myopericarditis-like syndrome of chest pain and normal or near-normal ventricular function because they can worsen cardiomyopathy in experimental models.<sup><span class="xrefLink" id="jumplink-EHR165C111"></span><a href="javascript:;" reveal-id="EHR165C111" data-open="EHR165C111" class="link link-ref link-reveal xref-bibr">111</a></sup> In addition to guideline-based medical management, we recommend that patients with acute myocarditis refrain from competitive athletics for a period of months after the acute infection or until ventricular recovery has been documented by non-invasive imaging.</p> <h3 scrollto-destination=6566934 id="6566934" class="section-title js-splitscreen-section-title" data-legacy-id=s4b>Antiviral treatment</h3> <h4 scrollto-destination=6566935 id="6566935" class="section-title js-splitscreen-section-title" data-legacy-id=s4b1>Treatment of early disease</h4> <p class="chapter-para">Elimination of viral translation, transcription, and proliferation with the use of antiviral medications that target viral attachment to host-cell receptors, virus entry, or virus uncoating, e.g. Pleconaril, WIN 54954, or soluble CAR-Fc, would be effective in the early stages, but, unfortunately, most adult patients present in the chronic phases of disease (<em>Figure <span class="xrefLink" id="jumplink-EHR165F1"></span><a href="javascript:;" data-modal-source-id="EHR165F1" class="link xref-fig">1</a></em>).<sup><span class="xrefLink" id="jumplink-EHR165C112"></span><a href="javascript:;" reveal-id="EHR165C112" data-open="EHR165C112" class="link link-ref link-reveal xref-bibr">112</a></sup> These agents, therefore, are of limited use in virus-associated heart disease. The current challenge of antiviral therapy in patients with <em>chronic</em> cardiac viral infections therefore is the timing of treatment that prevents progressive myocardial injury by viral clearance before chronically infected heart tissue has irreversible damage.</p> <h3 scrollto-destination=6566937 id="6566937" class="section-title js-splitscreen-section-title" data-legacy-id=s4c>Treatment of chronic viral heart disease</h3> <h4 scrollto-destination=6566938 id="6566938" class="section-title js-splitscreen-section-title" data-legacy-id=s4c1>Interferon-beta</h4> <p class="chapter-para">Interferons serve as a natural defense against many viral infections. Their innate production is associated with clinical recovery from viral infection and subsequent sequelae, while exogenous administration is protective. Type I interferons therefore constitute a promising choice for treatment of chronic viral cardiomyopathy. Currently, there is no approved treatment for chronic viral heart disease, but data from uncontrolled open labelled phase II studies have demonstrated that subgroups of patients, who had not improved upon regular heart failure medication, may get significant benefit even years after onset of chronic disease.</p><p class="chapter-para">In a first study, patients with persistent enterovirus and adenovirus infections of the myocardium responded well to a 6-months interferon-beta (IFN-β1a) course.<sup><span class="xrefLink" id="jumplink-EHR165C113"></span><a href="javascript:;" reveal-id="EHR165C113" data-open="EHR165C113" class="link link-ref link-reveal xref-bibr">113</a></sup> Complete elimination of enteroviral and adenoviral genome was proved by follow-up biopsies taken 3 month after termination of the antiviral therapy. Virus clearance was paralleled by an improvement of mean left ventricular function, a decrease in ventricular size, an amelioration of heart failure symptoms, and a decrease of infiltrating inflammatory cells. Of note, no patient deteriorated and patients with severely affected LV-dysfunction gained most benefit.<sup><span class="xrefLink" id="jumplink-EHR165C113"></span><a href="javascript:;" reveal-id="EHR165C113" data-open="EHR165C113" class="link link-ref link-reveal xref-bibr">113</a></sup></p><p class="chapter-para">The drug is usually administered subcutaneously every other day in addition to constant heart failure medication for a 6–months' period. In order to limit IFN-specific side effects, the patient should enter a run-in period to improve tolerance following a stepped regimen, during which the patient receives 2 × 10<sup>6</sup> IU IFN-β per application every other day for 1 week. Within the following 2 weeks, the study medication can be elevated to 4 × 10<sup>6</sup> and 6 × 10<sup>6</sup> IU IFN-β, respectively, and continued for the following 21 weeks. The IFN-β1a medication was well tolerated with no unexpected non-cardiologic or cardiologic side effects. Frequently reported IFN-associated side effects were fatigue, influenza-like symptoms, and injection site erythema but symptoms vanished regularly during the first 4 weeks of treatment. No major clinical events occurred during the treatment phase or follow-up.</p><p class="chapter-para">If patients with a severely depressed cardiac contractility (LVEF <25%) are treated with an immunmodulatory drug such as IFN-β, LV function should be close-mesh monitored by echocardiography. Between Week 4 and 12, patients complain for a mild aggravation of heart failure symptoms which is often associated with a wall oedema, a slight increase of LV-dimensions and a minor deterioration of LVEF. Complains regularly disappear within 1 or 2 weeks followed by an direct and continuous improvement of heart failure in ∼40% of patients. Improvement may start with a delay of for 2–4 months in 25–30% of patients. This outlined course, which is probably caused by an IFN-induced cellular immune response, preferentially concerns viruses that infect cardiomyocytes (e.g. enteroviruses). It is uncommonly observed in infections such as parvovirus B19 or human herpesvirus 6 which according to a distinct pathophysiology do not directly affect contractile cells of the myocardium.</p><p class="chapter-para">Parvovirus B19 and human herpes virus 6 respond less well upon IFN-β treatment with respect to virus clearance and haemodynamic changes, although affected patients too improve clinically despite incomplete virus clearance following reduction of virus load and/or improvement of endothelial dysfunction.<sup><span class="xrefLink" id="jumplink-EHR165C114"></span><a href="javascript:;" reveal-id="EHR165C114" data-open="EHR165C114" class="link link-ref link-reveal xref-bibr">114</a>,<span class="xrefLink" id="jumplink-EHR165C115"></span><a href="javascript:;" reveal-id="EHR165C115" data-open="EHR165C115" class="link link-ref link-reveal xref-bibr">115</a></sup> Complete clearance of those viruses may need longer treatment intervals, higher doses, or even a complete change of the antiviral treatment regimens. Currently, effective treatment conditions for viruses other than enterovirus and adenovirus have not yet been tested consequently.</p><p class="chapter-para">Information taken from uncontrolled cohorts of treated virus-positive patients may be, however, of limited value for general treatment recommendations for a number of reasons. According to animal and cell culture studies, different viruses and even different virus subtypes may respond in distinct and unpredictable ways to immunomodulatory treatment. Furthermore, virus load and the type of the infected cell, both of which influence course of the disease and drug response, have to be taken into consideration. Despite such comprehensible reservations, a recent randomized, placebo controlled phase II trial (BICC-Study) has confirmed that even patients with a long history who had not responded to conventional heart failure treatment can get clinical and haemodynamic benefit from an IFN therapy.<sup><span class="xrefLink" id="jumplink-EHR165C115"></span><a href="javascript:;" reveal-id="EHR165C115" data-open="EHR165C115" class="link link-ref link-reveal xref-bibr">115</a></sup></p><p class="chapter-para">Response to the IFN-β1a therapy may be influenced by the virus-associated local inflammation and the extent of the myocardial injury at the time when the specific therapy is started. The lack of haemodynamic improvement in some of the patients is not unexpected, if the long history and the above-mentioned pathogenetic suggestions are taken into consideration. In view of the information derived from other virus infections of the heart, one can expect that the chronic enteroviral and adenoviral infections or the virus-associated inflammatory process may already have caused considerable myocardial damage and consequently, ventricular dysfunction may be unable to recover completely in those patients who did not improve despite virus clearance. Nevertheless, the complete clearance of both viruses after treatment suggests that early biopsy-based diagnosis and timely treatment may prevent disease progression and thereby improve the outcome of chronic viral cardiomyopathy.</p><div id="" class="boxed-text boxed-matter no-caption"><p class="chapter-para"><em>Select knowledge gaps and opportunities in the treatment of myocarditis</em></p><p class="chapter-para">• Studies have not been done to determine when and how to discontinue standard heart failure therapy in patients who recovery LV function.</p><p class="chapter-para">• More work is needed to identify patient cohorts who will benefit from tailored antiviral or immunosuppressive therapy.</p><p class="chapter-para">• The optimal time frame to initiate immunosuppressive treatment improves cardiac function and health without impairment of a healing immune processes is unknown.</p><p class="chapter-para">• With respect to our limited knowledge of involved pathological processes and optimal treatment conditions, prevention of disease progression rather than curative treatment may turn out to be the most realistic short-term goal.</p></div> <h2 scrollto-destination=6566947 id="6566947" class="section-title js-splitscreen-section-title" data-legacy-id=s5>Immunosuppression</h2> <p class="chapter-para">Myocardial inflammatory processes due to pathogenic autoimmunity may survive myocardial virus elimination and warrant immunosuppressive treatment in order to prevent later immune-mediated myocardial injury.<sup><span class="xrefLink" id="jumplink-EHR165C116 EHR165C118"></span><a href="javascript:;" reveal-id="EHR165C116 EHR165C118" data-open="EHR165C116 EHR165C118" class="link link-ref link-reveal xref-bibr">116–118</a></sup> Immunosuppression demands biopsy-based exclusion of virus from treated patients since virus-positive patients do not improve upon anti-inflammatory treatment, while virus-negative patients with post-infectious or auto-immune inflammatory processes respond well in early clinical trials.<sup><span class="xrefLink" id="jumplink-EHR165C105"></span><a href="javascript:;" reveal-id="EHR165C105" data-open="EHR165C105" class="link link-ref link-reveal xref-bibr">105</a>,<span class="xrefLink" id="jumplink-EHR165C117"></span><a href="javascript:;" reveal-id="EHR165C117" data-open="EHR165C117" class="link link-ref link-reveal xref-bibr">117</a>,<span class="xrefLink" id="jumplink-EHR165C119"></span><a href="javascript:;" reveal-id="EHR165C119" data-open="EHR165C119" class="link link-ref link-reveal xref-bibr">119</a>,<span class="xrefLink" id="jumplink-EHR165C120"></span><a href="javascript:;" reveal-id="EHR165C120" data-open="EHR165C120" class="link link-ref link-reveal xref-bibr">120</a></sup></p><p class="chapter-para">Frequently administered anti-inflammatory drugs are immunoglobulins, corticosteroids, azathioprine, and cyclosporine, which are administered on top of regular heart failure medication. α-Methylprednisolone is generally given at Charite Hospital, at a dose of 1 mg/kg body weight, initially for 4 weeks. Depending on the body weight, azathioprine is administered at a dose of 100–150 mg daily in addition to the corticosteroid. The steroid dosage is titrated down every 2 weeks in increments of 10 mg until a maintenance dose of 10 mg is reached. The treatment duration should last for 3 to 6 months. Actual data of first randomized trials confirm efficacy of those treatment regimens in carefully selected patients.<sup><span class="xrefLink" id="jumplink-EHR165C105"></span><a href="javascript:;" reveal-id="EHR165C105" data-open="EHR165C105" class="link link-ref link-reveal xref-bibr">105</a>,<span class="xrefLink" id="jumplink-EHR165C118"></span><a href="javascript:;" reveal-id="EHR165C118" data-open="EHR165C118" class="link link-ref link-reveal xref-bibr">118</a></sup></p><p class="chapter-para">Sustained beneficial effects of immunosuppression on heart failure symptoms, left ventricular dimensions, and LVEF in immunohistologically biopsy-proven inflammatory cardiomyopathy have been confirmed in a randomized trial with 41 patients at 2 years follow-up after ≥3 months of treatment with corticosteroids and azathioprine.<sup><span class="xrefLink" id="jumplink-EHR165C118"></span><a href="javascript:;" reveal-id="EHR165C118" data-open="EHR165C118" class="link link-ref link-reveal xref-bibr">118</a></sup> This trial ultimately validates the diagnostic sensitivity and accuracy of cell adhesion molecule (CAM) abundance for indlammatory cardiomyopathy (DCMi) even in the absence of lymphocytic infiltration, possibly due to the close functional association between CAM induction and immunocompetent infiltration and cytokine induction,<sup><span class="xrefLink" id="jumplink-EHR165C121"></span><a href="javascript:;" reveal-id="EHR165C121" data-open="EHR165C121" class="link link-ref link-reveal xref-bibr">121</a></sup> and thus constitutes an important criterion for selecting those patients who will likely benefit from immunosuppression. Furthermore, this study showed that a 3-month regimen may equally be effective as previous trials that used 6 months of immunosuppression, and that beneficial effects last for an extended period of time (2 years). In another recently published randomized trial (TIMIC study), the authors confirmed a positive treatment response in patients with chronic active myocarditis.<sup><span class="xrefLink" id="jumplink-EHR165C105"></span><a href="javascript:;" reveal-id="EHR165C105" data-open="EHR165C105" class="link link-ref link-reveal xref-bibr">105</a></sup> Thirty-eight out of 43 patients on immunosuppressive therapy (88%) showed a improvement of cardiac function and dimensions, defined as an increase of >10 percentage points in the absolute EF and a reduction of LV end-diastolic volume (EDV) or LV end-diastolic diameter (EDD) 10% (i.e. LVEF from 26.4 ± 6.9 to 48.0 ± 7.3%, LVEDV from 258.0 ± 52.5 to 125.9 ± 29.6, and LVEDD from 68.6 ± 7.4 to 52.8 ± 6.3 mm). None of the untreated patients show at 6 month improvement of LVEF, that significantly worsened compared with baseline. In particular, 35 out of 42 patients (83%) showed further impairment of cardiac function (LVEF from 27.6 ± 6.6 to 19.5 ± 4.8, LVEDV from 244.7 ± 48.0 to 287.3 ± 48.0, and LVEDD from 69.2 ± 7.9 to 75.3 ± 7.4), while the remaining 7 patients remained stationary. Finally, LVEF declined to baseline (27.2 ± 5.6%) or lower (19.7 ± 4.4%) values.</p><p class="chapter-para">Currently available data show that immunosuppressive therapy in patients with biopsy-proven, virus-negative inflammatory cardiomyopathy is an effective and safe option in addition to supportive treatment for recovery of cardiac failure. However, larger studies powered to detect a difference in clinical endpoints such as heart failure hospitalization, transplantation, and death are still needed.</p> <h2 scrollto-destination=6566952 id="6566952" class="section-title js-splitscreen-section-title" data-legacy-id=s6>Intravenous immunoglobulin and immunoadsorption</h2> <p class="chapter-para">The first data of acute myocarditis treated with intravenous immunoglobulin (IVIG) suggested that use of high-dose IVIG for treatment of acute myocarditis is associated with improved recovery of left ventricular function and with a tendency to better survival during the first year after presentation.<sup><span class="xrefLink" id="jumplink-EHR165C122"></span><a href="javascript:;" reveal-id="EHR165C122" data-open="EHR165C122" class="link link-ref link-reveal xref-bibr">122</a></sup> Later investigations and randomized studies which compared IVIG and cortisone treatment revealed that the treatment with intravenous immune globulin in children was not effective.<sup><span class="xrefLink" id="jumplink-EHR165C123"></span><a href="javascript:;" reveal-id="EHR165C123" data-open="EHR165C123" class="link link-ref link-reveal xref-bibr">123</a></sup> Freedom from death or transplantation was 81% at 1 year, and 74% at 5 years, with no difference between the modes of treatments. The median time to recovery of function was also comparable between the groups. Thus, treatment with intravenous immune globulin appear to confer no advantage to steroid therapy alone.<sup><span class="xrefLink" id="jumplink-EHR165C124"></span><a href="javascript:;" reveal-id="EHR165C124" data-open="EHR165C124" class="link link-ref link-reveal xref-bibr">124</a></sup></p><p class="chapter-para">The rationale for immunoadsorption is to lower cardiotoxic antibodies in the patient's plasma, and with serial treatments over 5 or more days, extract antibodies and immune complexes from the heart as well. The plasma is separated from cellular components by a centrifuge or column and passed through an immunoadsorbtion column. IgG and to a lesser degree IgA and IgM are non-specifically adsorbed during repetitive sessions. Plasma IgG levels are partially restored by infusion of 0.5 g/kg polyclonal IgG >18 h after the last apheresis treatment. The favourable haemodynamic results of immunoadsorption in patients with DCMi may be related to removal of functionally active cardiac autoantibodies or other immunologically active compounds, since immunoadsorption leads to biopsy-proven decrease in lymphocytic infiltration and CAM expression.</p> <h2 scrollto-destination=6566955 id="6566955" class="section-title js-splitscreen-section-title" data-legacy-id=s7>Summary and perspectives</h2> <p class="chapter-para">Current pharmacological heart failure therapy of myocarditis-associated cardiomyopathy mainly focuses on decreasing the activity of the neuroendocrine system but does not directly influence virus-induced inflammatory cardiomyopathy. Interferon-β suppresses erythrovirus replication while at the same time it improves replication and viability of human ECs.<sup><span class="xrefLink" id="jumplink-EHR165C46"></span><a href="javascript:;" reveal-id="EHR165C46" data-open="EHR165C46" class="link link-ref link-reveal xref-bibr">46</a></sup> Accumulating experimental and clinical data indicate that cellular transplantation may improve myocardial function.<sup><span class="xrefLink" id="jumplink-EHR165C26"></span><a href="javascript:;" reveal-id="EHR165C26" data-open="EHR165C26" class="link link-ref link-reveal xref-bibr">26</a>,<span class="xrefLink" id="jumplink-EHR165C125"></span><a href="javascript:;" reveal-id="EHR165C125" data-open="EHR165C125" class="link link-ref link-reveal xref-bibr">125</a>,<span class="xrefLink" id="jumplink-EHR165C126"></span><a href="javascript:;" reveal-id="EHR165C126" data-open="EHR165C126" class="link link-ref link-reveal xref-bibr">126</a></sup> Mesenchymal stem cells (MSCs) have anti-apoptotic, anti-fibrotic properties, are non-immunogenic, and possess immunomodulatory properties.<sup><span class="xrefLink" id="jumplink-EHR165C127 EHR165C129"></span><a href="javascript:;" reveal-id="EHR165C127 EHR165C129" data-open="EHR165C127 EHR165C129" class="link link-ref link-reveal xref-bibr">127–129</a></sup> They suppress T-cell responses, induce apoptosis of activated T cells and increase T regulatory cells.<sup><span class="xrefLink" id="jumplink-EHR165C130 EHR165C132"></span><a href="javascript:;" reveal-id="EHR165C130 EHR165C132" data-open="EHR165C130 EHR165C132" class="link link-ref link-reveal xref-bibr">130–132</a></sup> Interferon-γ primes MSC-mediated immunoregulatory effects and induces nitric oxide (NO) production in MSCs the latter of which exerts anti-apoptotic effects on cardiomyocytes and has antiviral properties in a NO-dependent manner.<sup><span class="xrefLink" id="jumplink-EHR165C129"></span><a href="javascript:;" reveal-id="EHR165C129" data-open="EHR165C129" class="link link-ref link-reveal xref-bibr">129</a>,<span class="xrefLink" id="jumplink-EHR165C133 EHR165C135"></span><a href="javascript:;" reveal-id="EHR165C133 EHR165C135" data-open="EHR165C133 EHR165C135" class="link link-ref link-reveal xref-bibr">133–135</a></sup> These different strategies including pharmacological and gene therapeutic approaches directed at blocking viral replication or stimulating the antiviral-directed immune response, are under investigation in experimental and clinical studies.<sup><span class="xrefLink" id="jumplink-EHR165C70"></span><a href="javascript:;" reveal-id="EHR165C70" data-open="EHR165C70" class="link link-ref link-reveal xref-bibr">70</a>,<span class="xrefLink" id="jumplink-EHR165C114"></span><a href="javascript:;" reveal-id="EHR165C114" data-open="EHR165C114" class="link link-ref link-reveal xref-bibr">114</a>,<span class="xrefLink" id="jumplink-EHR165C136"></span><a href="javascript:;" reveal-id="EHR165C136" data-open="EHR165C136" class="link link-ref link-reveal xref-bibr">136</a>,<span class="xrefLink" id="jumplink-EHR165C137"></span><a href="javascript:;" reveal-id="EHR165C137" data-open="EHR165C137" class="link link-ref link-reveal xref-bibr">137</a></sup> Because of the low rate of diagnosis, multi-centre collaborations with standardized evaluations and treatment protocols, mechanistically oriented registries, and core molecular diagnostic facilities will be needed.</p> <h2 scrollto-destination=6566957 id="6566957" class="section-title js-splitscreen-section-title" data-legacy-id=s8>Funding</h2> <p class="chapter-para">Basic experimental diagnostic and clinical works have been supported by a grant from the German Research Foundation (DFG), Transregional Collaborative Research Centre ‘Inflammatory Cardiomyopathy–Molecular Pathogenesis and Therapy’ (SFB TR 19 04) (HPS, UK, Charite Berlin).</p><p class="chapter-para"><strong>Conflict of interest</strong>: none declared.</p> <h2 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