Skip to main content
Top
Published in: Heart Failure Reviews 6/2013

01-11-2013

Viral myocarditis: from experimental models to molecular diagnosis in patients

Authors: Sabine Pankuweit, Karin Klingel

Published in: Heart Failure Reviews | Issue 6/2013

Login to get access

Abstract

Cardiotropic viruses have been implicated as major pathogenetic agents in acute and chronic forms of myocarditis. By the introduction of molecular tools, such as (RT-) polymerase chain reaction ((RT-) PCR) and in situ hybridization in the diagnosis of inflammatory heart disease, genomes of various RNA and DNA viruses comprising enteroviruses, adenoviruses, parvovirus B19 (B19V) and herpesviruses (EBV, HHV6, HCMV) were detected in endomyocardial biopsies of patients with myocarditis and dilated cardiomyopathy. Meanwhile, it is known that the outcome of a virus infection in the heart resulting in myocarditis is determined by genetic host factors as well as by the viral pathogenicity which considerably varies in the different virus infections. A considerable portion of our knowledge about the etiopathogenetic mechanisms in viral heart disease is derived from animal studies. Whereas the evolvement of cardiac inflammation in enterovirus infections is guided by viral cytotoxicity and virus persistence, in herpesvirus infections, the pathophysiology is rather determined by primary immune-mediated pathogenicity. By investigation of immunocompetent and gene-targeted mice, valuable new insights into host and virus factors relevant for the control of cardiac viral infection and inflammation were gained which are reviewed in this paper.
Literature
1.
go back to reference Kühl U, Pauschinger M, Seeberg B, Lassner D, Noutsias M, Poller W, Schultheiss HP (2005) Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 112:1965–1970PubMed Kühl U, Pauschinger M, Seeberg B, Lassner D, Noutsias M, Poller W, Schultheiss HP (2005) Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 112:1965–1970PubMed
2.
go back to reference Kindermann I, Kindermann M, Kandolf R, Klingel K, Bültmann B, Müller T et al (2008) Predictors of outcome in patients with suspected myocarditis. Circulation 118:639–648PubMed Kindermann I, Kindermann M, Kandolf R, Klingel K, Bültmann B, Müller T et al (2008) Predictors of outcome in patients with suspected myocarditis. Circulation 118:639–648PubMed
3.
go back to reference Schultz JC, Hilliard AA, Cooper LT Jr, Rihal CS (2009) Diagnosis and treatment of viral myocarditis. Mayo Clin Proc 84:1001–1009PubMed Schultz JC, Hilliard AA, Cooper LT Jr, Rihal CS (2009) Diagnosis and treatment of viral myocarditis. Mayo Clin Proc 84:1001–1009PubMed
4.
go back to reference Bock CT, Klingel K, Kandolf R (2010) Human parvovirus B19-associated myocarditis. N Engl J Med 362:1248–1249PubMed Bock CT, Klingel K, Kandolf R (2010) Human parvovirus B19-associated myocarditis. N Engl J Med 362:1248–1249PubMed
5.
go back to reference Ruppert V, Meyer T, Balbach A, Richter A, Müller HH, Maisch B, Pankuweit S (2011) German heart failure network. Genotype-specific effects on left ventricular function in parvovirus B19-positive patients with dilated cardiomyopathy. J Med Virol 83:1818–1825PubMed Ruppert V, Meyer T, Balbach A, Richter A, Müller HH, Maisch B, Pankuweit S (2011) German heart failure network. Genotype-specific effects on left ventricular function in parvovirus B19-positive patients with dilated cardiomyopathy. J Med Virol 83:1818–1825PubMed
6.
go back to reference Gdynia G, Schnitzler P, Brunner E, Kandolf R, Bläker H, Daum E, Schnabel P, Schirmacher P, Roth W (2011) Sudden death of an immunocompetent young adult caused by novel (swine origin) influenza A/H1N1-associated myocarditis. Virchows Arch 458:371–376PubMed Gdynia G, Schnitzler P, Brunner E, Kandolf R, Bläker H, Daum E, Schnabel P, Schirmacher P, Roth W (2011) Sudden death of an immunocompetent young adult caused by novel (swine origin) influenza A/H1N1-associated myocarditis. Virchows Arch 458:371–376PubMed
7.
go back to reference Barbaro G (2005) HIV-associated myocarditis. Heart Fail Clin 1:439–448 (Review)PubMed Barbaro G (2005) HIV-associated myocarditis. Heart Fail Clin 1:439–448 (Review)PubMed
8.
go back to reference Esfandiarei M, McManus BM (2008) Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol Mech Dis 3:127–155 (Review) Esfandiarei M, McManus BM (2008) Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol Mech Dis 3:127–155 (Review)
9.
go back to reference Kandolf R, Klingel K, Mertsching H, Canu A, Hohenadl C, Zell R, Reimann BY, Heim A, McManus BM, Foulis AK et al (1991) Molecular studies on enteroviral heart disease: patterns of acute and persistent infections. Eur Heart J 12(Suppl D):49–55 (Review)PubMed Kandolf R, Klingel K, Mertsching H, Canu A, Hohenadl C, Zell R, Reimann BY, Heim A, McManus BM, Foulis AK et al (1991) Molecular studies on enteroviral heart disease: patterns of acute and persistent infections. Eur Heart J 12(Suppl D):49–55 (Review)PubMed
10.
go back to reference Klingel K, Rieger P, Mall G, Selinka HC, Huber M, Kandolf R (1998) Visualization of enteroviral replication in myocardial tissue by ultrastructural in situ hybridization: identification of target cells and cytopathic effects. Lab Invest 78:1227–1237PubMed Klingel K, Rieger P, Mall G, Selinka HC, Huber M, Kandolf R (1998) Visualization of enteroviral replication in myocardial tissue by ultrastructural in situ hybridization: identification of target cells and cytopathic effects. Lab Invest 78:1227–1237PubMed
11.
go back to reference McManus BM, Chow LH, Wilson JE, Anderson DR, Gulizia JM, Gauntt CJ, Klingel KE, Beisel KW, Kandolf R (1993) Direct myocardial injury by enterovirus: a central role in the evolution of murine myocarditis. Clin Immunol Immunopathol 68:159–169PubMed McManus BM, Chow LH, Wilson JE, Anderson DR, Gulizia JM, Gauntt CJ, Klingel KE, Beisel KW, Kandolf R (1993) Direct myocardial injury by enterovirus: a central role in the evolution of murine myocarditis. Clin Immunol Immunopathol 68:159–169PubMed
12.
go back to reference Jahns R, Boivin V, Hein L, Triebel S, Angermann CE, Ertl G, Lohse MJ (2004) Direct evidence for a beta1-adrenergic receptor-directed autoimmune attack as a cause of idiopathic dilated Cardiomyopathy. J Clin Invest 113:1419–1429PubMed Jahns R, Boivin V, Hein L, Triebel S, Angermann CE, Ertl G, Lohse MJ (2004) Direct evidence for a beta1-adrenergic receptor-directed autoimmune attack as a cause of idiopathic dilated Cardiomyopathy. J Clin Invest 113:1419–1429PubMed
13.
go back to reference Caforio AL, Tona F, Bottaro S, Vinci A, Dequal G, Daliento L, Thiene G, Iliceto S (2008) Clinical implications of anti-heart autoantibodies in myocarditis and dilated cardiomyopathy. Autoimmunity 41(1):35–45 (Review)PubMed Caforio AL, Tona F, Bottaro S, Vinci A, Dequal G, Daliento L, Thiene G, Iliceto S (2008) Clinical implications of anti-heart autoantibodies in myocarditis and dilated cardiomyopathy. Autoimmunity 41(1):35–45 (Review)PubMed
14.
go back to reference Ogata M, Satou T, Kawano R, Takakura S, Goto K, Ikewaki J, Kohno K, Ikebe T, Ando T, Miyazaki Y, Ohtsuka E, Saburi Y, Saikawa T, Kadota J (2010) Correlations of HHV-6 viral load and plasma IL-6 concentration with HHV-6 encephalitis in allogeneic stem cell transplant recipients. Bone Marrow Transpl 45:129–136 Ogata M, Satou T, Kawano R, Takakura S, Goto K, Ikewaki J, Kohno K, Ikebe T, Ando T, Miyazaki Y, Ohtsuka E, Saburi Y, Saikawa T, Kadota J (2010) Correlations of HHV-6 viral load and plasma IL-6 concentration with HHV-6 encephalitis in allogeneic stem cell transplant recipients. Bone Marrow Transpl 45:129–136
15.
go back to reference Klingel K, Hohenadl C, Canu A, Albrecht M, Seemann M, Mall G, Kandolf R (1992) Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc Natl Acad Sci USA 89:314–318PubMed Klingel K, Hohenadl C, Canu A, Albrecht M, Seemann M, Mall G, Kandolf R (1992) Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc Natl Acad Sci USA 89:314–318PubMed
16.
go back to reference Shi Y, Chen C, Lisewski U, Wrackmeyer U, Radke M, Westermann D, Sauter M, Tschöpe C, Poller W, Klingel K, Gotthardt M (2009) Cardiac deletion of the Coxsackievirus-adenovirus receptor abolishes Coxsackievirus B3 infection and prevents myocarditis in vivo. J Am Coll Cardiol 53:1219–1226PubMed Shi Y, Chen C, Lisewski U, Wrackmeyer U, Radke M, Westermann D, Sauter M, Tschöpe C, Poller W, Klingel K, Gotthardt M (2009) Cardiac deletion of the Coxsackievirus-adenovirus receptor abolishes Coxsackievirus B3 infection and prevents myocarditis in vivo. J Am Coll Cardiol 53:1219–1226PubMed
17.
go back to reference Herzum M, Ruppert V, Küytz B, Jomaa H, Nakamura I, Maisch B (1994) Coxsackievirus B3 infection leads to cell death of cardiac myocytes. J Mol Cell Cardiol 26:907–913PubMed Herzum M, Ruppert V, Küytz B, Jomaa H, Nakamura I, Maisch B (1994) Coxsackievirus B3 infection leads to cell death of cardiac myocytes. J Mol Cell Cardiol 26:907–913PubMed
18.
go back to reference Chow LH, Beisel KW, McManus BM (1992) Enteroviral infection of mice with severe combined immunodeficiency. Evidence for direct viral pathogenesis of myocardial injury. Lab Invest 66:24–31PubMed Chow LH, Beisel KW, McManus BM (1992) Enteroviral infection of mice with severe combined immunodeficiency. Evidence for direct viral pathogenesis of myocardial injury. Lab Invest 66:24–31PubMed
19.
go back to reference Wessely R, Klingel K, Santana LF, Dalton N, Hongo M, Jonathan Lederer W, Kandolf R, Knowlton KU (1998) Transgenic expression of replication-restricted enteroviral genomes in heart muscle induces defective excitation-contraction coupling and dilated cardiomyopathy. J Clin Invest 102:1444–1453PubMed Wessely R, Klingel K, Santana LF, Dalton N, Hongo M, Jonathan Lederer W, Kandolf R, Knowlton KU (1998) Transgenic expression of replication-restricted enteroviral genomes in heart muscle induces defective excitation-contraction coupling and dilated cardiomyopathy. J Clin Invest 102:1444–1453PubMed
20.
go back to reference Badorff C, Lee GH, Lamphear BJ et al (1999) Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat Med 5:320–326PubMed Badorff C, Lee GH, Lamphear BJ et al (1999) Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat Med 5:320–326PubMed
21.
go back to reference Luo H, Zhang J, Cheung C, Suarez A, McManus BM, Yang D (2003) Proteasome inhibition reduces coxsackievirus B3 replication in murine cardiomyocytes. Am J Pathol 163:381–385PubMed Luo H, Zhang J, Cheung C, Suarez A, McManus BM, Yang D (2003) Proteasome inhibition reduces coxsackievirus B3 replication in murine cardiomyocytes. Am J Pathol 163:381–385PubMed
22.
go back to reference Esfandiarei M, Suarez A, Amaral A, Si X, Rahmani M, Dedhar S, McManus BM (2006) Novel role for integrin-linked kinase in modulation of coxsackievirus B3 replication and virus-induced cardiomyocyte injury. Circ Res 99:354–361PubMed Esfandiarei M, Suarez A, Amaral A, Si X, Rahmani M, Dedhar S, McManus BM (2006) Novel role for integrin-linked kinase in modulation of coxsackievirus B3 replication and virus-induced cardiomyocyte injury. Circ Res 99:354–361PubMed
23.
go back to reference Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H (2008) Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 82:9143–9153PubMed Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H (2008) Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 82:9143–9153PubMed
24.
go back to reference Wessely R, Klingel K, Knowlton KU, Kandolf R (2001) Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 103:756–761PubMed Wessely R, Klingel K, Knowlton KU, Kandolf R (2001) Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication. Circulation 103:756–761PubMed
25.
go back to reference Deonarain R, Cerullo D, Fuse K, Liu PP, Fish EN (2004) Protective role for interferon-beta in coxsackievirus B3 infection. Circulation 110:3540–3543PubMed Deonarain R, Cerullo D, Fuse K, Liu PP, Fish EN (2004) Protective role for interferon-beta in coxsackievirus B3 infection. Circulation 110:3540–3543PubMed
26.
go back to reference Weinzierl AO, Szalay G, Wolburg H, Sauter M, Rammensee HG, Kandolf R, Stevanović S, Klingel K (2008) Effective chemokine secretion by dendritic cells and expansion of cross-presenting CD4-/CD8+ dendritic cells define a protective phenotype in the mouse model of coxsackievirus myocarditis. J Virol 82:8149–8160PubMed Weinzierl AO, Szalay G, Wolburg H, Sauter M, Rammensee HG, Kandolf R, Stevanović S, Klingel K (2008) Effective chemokine secretion by dendritic cells and expansion of cross-presenting CD4-/CD8+ dendritic cells define a protective phenotype in the mouse model of coxsackievirus myocarditis. J Virol 82:8149–8160PubMed
27.
go back to reference Riad A, Westermann D, Escher F, Becher PM, Savvatis K, Lettau O, Heimesaat MM, Bereswill S, Volk HD, Schultheiss HP, Tschöpe C (2010) Myeloid differentiation factor-88 contributes to TLR9-mediated modulation of acute coxsackievirus B3-induced myocarditis in vivo. Am J Physiol Heart Circ Physiol 298(6):H2024–H2031PubMed Riad A, Westermann D, Escher F, Becher PM, Savvatis K, Lettau O, Heimesaat MM, Bereswill S, Volk HD, Schultheiss HP, Tschöpe C (2010) Myeloid differentiation factor-88 contributes to TLR9-mediated modulation of acute coxsackievirus B3-induced myocarditis in vivo. Am J Physiol Heart Circ Physiol 298(6):H2024–H2031PubMed
28.
go back to reference Klingel K, Schnorr JJ, Sauter M, Szalay G, Kandolf R (2003) beta2-microglobulin-associated regulation of interferon-gamma and virus-specific immunoglobulin G confer resistance against the development of chronic coxsackievirus myocarditis. Am J Pathol 162:1709–1720PubMed Klingel K, Schnorr JJ, Sauter M, Szalay G, Kandolf R (2003) beta2-microglobulin-associated regulation of interferon-gamma and virus-specific immunoglobulin G confer resistance against the development of chronic coxsackievirus myocarditis. Am J Pathol 162:1709–1720PubMed
29.
go back to reference Opavsky MA, Penninger J, Aitken K, Wen WH, Dawood F, Mak T, Liu P (1999) Susceptibility to myocarditis is dependent on the response of alphabeta T lymphocytes to coxsackieviral infection. Circ Res 85:551–558PubMed Opavsky MA, Penninger J, Aitken K, Wen WH, Dawood F, Mak T, Liu P (1999) Susceptibility to myocarditis is dependent on the response of alphabeta T lymphocytes to coxsackieviral infection. Circ Res 85:551–558PubMed
30.
go back to reference Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J, Whitton JL (1999) The role of B lymphocytes in coxsackievirus B3 infection. Am J Pathol 155:1205–1215PubMed Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J, Whitton JL (1999) The role of B lymphocytes in coxsackievirus B3 infection. Am J Pathol 155:1205–1215PubMed
31.
go back to reference Frisancho-Kiss S, Coronado MJ, Frisancho JA, Lau VM, Rose NR, Klein SL, Fairweather D (2009) Gonadectomy of male BALB/c mice increases Tim-3(+) alternatively activated M2 macrophages, Tim-3(+) T cells, Th2 cells and Treg in the heart during acute coxsackievirus-induced myocarditis. Brain Behav Immun 23:649–657PubMed Frisancho-Kiss S, Coronado MJ, Frisancho JA, Lau VM, Rose NR, Klein SL, Fairweather D (2009) Gonadectomy of male BALB/c mice increases Tim-3(+) alternatively activated M2 macrophages, Tim-3(+) T cells, Th2 cells and Treg in the heart during acute coxsackievirus-induced myocarditis. Brain Behav Immun 23:649–657PubMed
32.
go back to reference Szalay G, Sauter M, Hald J, Weinzierl A, Kandolf R, Klingel K (2006) Sustained nitric oxide synthesis contributes to immunopathology in ongoing myocarditis attributable to interleukin-10 disorders. Am J Pathol 169:2085–2093PubMed Szalay G, Sauter M, Hald J, Weinzierl A, Kandolf R, Klingel K (2006) Sustained nitric oxide synthesis contributes to immunopathology in ongoing myocarditis attributable to interleukin-10 disorders. Am J Pathol 169:2085–2093PubMed
33.
go back to reference Li K, Xu W, Guo Q, Jiang Z, Wang P, Yue Y, Xiong S (2009) Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res 105:353–364PubMed Li K, Xu W, Guo Q, Jiang Z, Wang P, Yue Y, Xiong S (2009) Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res 105:353–364PubMed
34.
go back to reference Cheung C, Luo H, Yanagawa B, Leong HS, Samarasekera D, Lai JC, Suarez A, Zhang J, McManus BM (2006) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in coxsackievirus-induced myocarditis. Cardiovasc Pathol 15:63–74PubMed Cheung C, Luo H, Yanagawa B, Leong HS, Samarasekera D, Lai JC, Suarez A, Zhang J, McManus BM (2006) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in coxsackievirus-induced myocarditis. Cardiovasc Pathol 15:63–74PubMed
35.
go back to reference Cheung C, Marchant D, Walker EK, Luo Z, Zhang J, Yanagawa B, Rahmani M, Cox J, Overall C, Senior RM, Luo H, McManus BM (2008) Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation 117:1574–1582PubMed Cheung C, Marchant D, Walker EK, Luo Z, Zhang J, Yanagawa B, Rahmani M, Cox J, Overall C, Senior RM, Luo H, McManus BM (2008) Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation 117:1574–1582PubMed
36.
go back to reference Heymans S, Pauschinger M, De Palma A, Kallwellis-Opara A, Rutschow S, Swinnen M, Vanhoutte D, Gao F, Torpai R, Baker AH, Padalko E, Neyts J, Schultheiss HP, Van de Werf F, Carmeliet P, Pinto YM (2006) Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis. Circulation 114:565–573PubMed Heymans S, Pauschinger M, De Palma A, Kallwellis-Opara A, Rutschow S, Swinnen M, Vanhoutte D, Gao F, Torpai R, Baker AH, Padalko E, Neyts J, Schultheiss HP, Van de Werf F, Carmeliet P, Pinto YM (2006) Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis. Circulation 114:565–573PubMed
37.
go back to reference Szalay G, Sauter M, Haberland M, Zuegel U, Steinmeyer A, Kandolf R, Klingel K (2009) Osteopontin: a fibrosis-related marker molecule in cardiac remodeling of enterovirus myocarditis in the susceptible host. Circ Res 104:851–859PubMed Szalay G, Sauter M, Haberland M, Zuegel U, Steinmeyer A, Kandolf R, Klingel K (2009) Osteopontin: a fibrosis-related marker molecule in cardiac remodeling of enterovirus myocarditis in the susceptible host. Circ Res 104:851–859PubMed
38.
go back to reference Lang C, Sauter M, Szalay G, Racchi G, Grassi G, Rainaldi G, Mercatanti A, Lang F, Kandolf R, Klingel K (2008) Connective tissue growth factor: a crucial cytokine-mediating cardiac fibrosis in ongoing enterovirus myocarditis. J Mol Med (Berl) 86:49–60 Lang C, Sauter M, Szalay G, Racchi G, Grassi G, Rainaldi G, Mercatanti A, Lang F, Kandolf R, Klingel K (2008) Connective tissue growth factor: a crucial cytokine-mediating cardiac fibrosis in ongoing enterovirus myocarditis. J Mol Med (Berl) 86:49–60
39.
go back to reference Rother M, Krohn S, Kania G, Vanhoutte D, Eisenreich A, Wang X, Westermann D, Savvatis K, Dannemann N, Skurk C, Hilfiker-Kleiner D, Cathomen T, Fechner H, Rauch U, Schultheiss HP, Heymans S, Eriksson U, Scheibenbogen C, Poller W (2010) Matricellular signaling molecule CCN1 attenuates experimental autoimmune myocarditis by acting as a novel immune cell migration modulator. Circulation 122:2688–2698PubMed Rother M, Krohn S, Kania G, Vanhoutte D, Eisenreich A, Wang X, Westermann D, Savvatis K, Dannemann N, Skurk C, Hilfiker-Kleiner D, Cathomen T, Fechner H, Rauch U, Schultheiss HP, Heymans S, Eriksson U, Scheibenbogen C, Poller W (2010) Matricellular signaling molecule CCN1 attenuates experimental autoimmune myocarditis by acting as a novel immune cell migration modulator. Circulation 122:2688–2698PubMed
40.
go back to reference Cunningham MW (2004) T cell mimicry in inflammatory heart disease. Mol Immunol 40:1121–1127PubMed Cunningham MW (2004) T cell mimicry in inflammatory heart disease. Mol Immunol 40:1121–1127PubMed
41.
go back to reference Li Y, Heuser JS, Cunningham LC et al (2006) Mimicry and antibody-mediated cell signaling in autoimmune myocarditis. J Immunol 177:8234–8240PubMed Li Y, Heuser JS, Cunningham LC et al (2006) Mimicry and antibody-mediated cell signaling in autoimmune myocarditis. J Immunol 177:8234–8240PubMed
42.
go back to reference Fousteri G, Dave A, Morin B, Omid S, Croft M, von Herrath MG (2011) Nasal cardiac myosin peptide treatment and OX40 blockade protect mice from acute and chronic virally-induced myocarditis. J Autoimmun 36:210–220PubMed Fousteri G, Dave A, Morin B, Omid S, Croft M, von Herrath MG (2011) Nasal cardiac myosin peptide treatment and OX40 blockade protect mice from acute and chronic virally-induced myocarditis. J Autoimmun 36:210–220PubMed
43.
go back to reference Masek-Hammerman K, Miller AD, Lin KC, Mackey J, Weissenböck H, Gierbolini L, Burgos A, Perez H, Mansfield KG. (2011) Epizootic myocarditis associated with encephalomyocarditis virus in a group of rhesus macaques (Macacamulatta). Vet Pathol 28 [Epub ahead of print] Masek-Hammerman K, Miller AD, Lin KC, Mackey J, Weissenböck H, Gierbolini L, Burgos A, Perez H, Mansfield KG. (2011) Epizootic myocarditis associated with encephalomyocarditis virus in a group of rhesus macaques (Macacamulatta). Vet Pathol 28 [Epub ahead of print]
44.
go back to reference Oberste MS, Gotuzzo E, Blair P, Nix WA, Ksiazek TG, Comer JA, Rollin P, Goldsmith CS, Olson J, Kochel TJ (2009) Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg Infect Dis 15:640–646PubMed Oberste MS, Gotuzzo E, Blair P, Nix WA, Ksiazek TG, Comer JA, Rollin P, Goldsmith CS, Olson J, Kochel TJ (2009) Human febrile illness caused by encephalomyocarditis virus infection, Peru. Emerg Infect Dis 15:640–646PubMed
45.
go back to reference Hardarson HS, Baker JS, Yang Z, Purevjav E, Huang CH, Alexopoulou L, Li N, Flavell RA, Bowles NE, Vallejo JG (2007) Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am J Physiol Heart Circ Physiol 292:H251–H258PubMed Hardarson HS, Baker JS, Yang Z, Purevjav E, Huang CH, Alexopoulou L, Li N, Flavell RA, Bowles NE, Vallejo JG (2007) Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am J Physiol Heart Circ Physiol 292:H251–H258PubMed
46.
go back to reference Yamada T, Matsumori A, Sasayama S (1994) Therapeutic effect of anti-tumor necrosis factor-alpha antibody on the murine model of viral myocarditis induced by encephalomyocarditis virus. Circulation 89:846–851PubMed Yamada T, Matsumori A, Sasayama S (1994) Therapeutic effect of anti-tumor necrosis factor-alpha antibody on the murine model of viral myocarditis induced by encephalomyocarditis virus. Circulation 89:846–851PubMed
47.
go back to reference Tanaka T, Kanda T, McManus BM, Kanai H, Akiyama H, Sekiguchi K, Yokoyama T, Kurabayashi M (2001) Overexpression of interleukin-6 aggravates viral myocarditis: impaired increase in tumor necrosis factor-alpha. J Mol Cell Cardiol 33:1627–1635PubMed Tanaka T, Kanda T, McManus BM, Kanai H, Akiyama H, Sekiguchi K, Yokoyama T, Kurabayashi M (2001) Overexpression of interleukin-6 aggravates viral myocarditis: impaired increase in tumor necrosis factor-alpha. J Mol Cell Cardiol 33:1627–1635PubMed
48.
go back to reference Higuchi H, Hara M, Yamamoto K, Miyamoto T, Kinoshita M, Yamada T, Uchiyama K, Matsumori A (2008) Mast cells play a critical role in the pathogenesis of viral myocarditis. Circulation 118:363–372PubMed Higuchi H, Hara M, Yamamoto K, Miyamoto T, Kinoshita M, Yamada T, Uchiyama K, Matsumori A (2008) Mast cells play a critical role in the pathogenesis of viral myocarditis. Circulation 118:363–372PubMed
49.
go back to reference Huang CH, Vallejo JG, Kollias G, Mann DL (2009) Role of the innate immune system in acute viral myocarditis. Basic Res Cardiol 104:228–237PubMed Huang CH, Vallejo JG, Kollias G, Mann DL (2009) Role of the innate immune system in acute viral myocarditis. Basic Res Cardiol 104:228–237PubMed
50.
go back to reference Takahashi T, Zhu SJ, Sumino H, Saegusa S, Nakahashi T, Iwai K, Morimoto S, Kanda T (2005) Inhibition of cyclooxygenase-2 enhances myocardial damage in a mouse model of viral myocarditis. Life Sci 78:195–204PubMed Takahashi T, Zhu SJ, Sumino H, Saegusa S, Nakahashi T, Iwai K, Morimoto S, Kanda T (2005) Inhibition of cyclooxygenase-2 enhances myocardial damage in a mouse model of viral myocarditis. Life Sci 78:195–204PubMed
51.
go back to reference Matsumori A (2007) Treatment options in myocarditis: what we know from experimental data and how it translates to clinical trials. Herz 32:452–456 (Review)PubMed Matsumori A (2007) Treatment options in myocarditis: what we know from experimental data and how it translates to clinical trials. Herz 32:452–456 (Review)PubMed
52.
go back to reference Sherry B, Li XY, Tyler KL, Cullen JM, Virgin HW 4th (1993) Lymphocytes protect against and are not required for reovirus-induced myocarditis. J Virol 67:6119–6124PubMed Sherry B, Li XY, Tyler KL, Cullen JM, Virgin HW 4th (1993) Lymphocytes protect against and are not required for reovirus-induced myocarditis. J Virol 67:6119–6124PubMed
53.
go back to reference Sherry B, Baty CJ, Blum MA (1996) Reovirus-induced acute myocarditis in mice correlates with viral RNA synthesis rather than generation of infectious virus in cardiac myocytes. J Virol 70:6709–6715PubMed Sherry B, Baty CJ, Blum MA (1996) Reovirus-induced acute myocarditis in mice correlates with viral RNA synthesis rather than generation of infectious virus in cardiac myocytes. J Virol 70:6709–6715PubMed
54.
go back to reference Sherry B, Torres J, Blum MA (1998) Reovirus induction of and sensitivity to beta interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J Virol 72:1314–1323PubMed Sherry B, Torres J, Blum MA (1998) Reovirus induction of and sensitivity to beta interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J Virol 72:1314–1323PubMed
55.
go back to reference Virgin HW, Dermody TS, Tyler KL (1998) Cellular and humoral immunity to reovirus infection. Curr Top Microbiol Immunol 233:147–161 (Review)PubMed Virgin HW, Dermody TS, Tyler KL (1998) Cellular and humoral immunity to reovirus infection. Curr Top Microbiol Immunol 233:147–161 (Review)PubMed
56.
go back to reference Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB (2004) Does Toll-like receptor 3 play a biological role in virus infections? Virology 322:231–238PubMed Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB (2004) Does Toll-like receptor 3 play a biological role in virus infections? Virology 322:231–238PubMed
57.
go back to reference Holm GH, Zurney J, Tumilasci V, Leveille S, Danthi P, Hiscott J, Sherry B, Dermody TS (2007) Retinoic acid-inducible gene-I and interferon-beta promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J Biol Chem 282:21953–21961PubMed Holm GH, Zurney J, Tumilasci V, Leveille S, Danthi P, Hiscott J, Sherry B, Dermody TS (2007) Retinoic acid-inducible gene-I and interferon-beta promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J Biol Chem 282:21953–21961PubMed
58.
go back to reference O’Donnell SM, Holm GH, Pierce JM, Tian B, Watson MJ, Chari RS, Ballard DW, Brasier AR, Dermody TS (2006) Identification of an NF-kappaB-dependent gene network in cells infected by mammalian reovirus. J Virol 80:1077–1086PubMed O’Donnell SM, Holm GH, Pierce JM, Tian B, Watson MJ, Chari RS, Ballard DW, Brasier AR, Dermody TS (2006) Identification of an NF-kappaB-dependent gene network in cells infected by mammalian reovirus. J Virol 80:1077–1086PubMed
59.
go back to reference Holm GH, Pruijssers AJ, Li L, Danthi P, Sherry B, Dermody TS (2010) Interferon regulatory factor 3 attenuates reovirus myocarditis and contributes to viral clearance. J Virol 84:6900–6908PubMed Holm GH, Pruijssers AJ, Li L, Danthi P, Sherry B, Dermody TS (2010) Interferon regulatory factor 3 attenuates reovirus myocarditis and contributes to viral clearance. J Virol 84:6900–6908PubMed
60.
go back to reference Li L, Sevinsky JR, Rowland MD, Bundy JL, Stephenson JL, Sherry B (2010) Proteomic analysis reveals virus-specific Hsp25 modulation in cardiac myocytes. J Proteome Res 9:2460–2471PubMed Li L, Sevinsky JR, Rowland MD, Bundy JL, Stephenson JL, Sherry B (2010) Proteomic analysis reveals virus-specific Hsp25 modulation in cardiac myocytes. J Proteome Res 9:2460–2471PubMed
61.
go back to reference Miyamoto SD, Brown RD, Robinson BA, Tyler KL, Long CS, Debiasi RL (2009) Cardiac cell-specific apoptotic and cytokine responses to reovirus infection: determinants of myocarditic phenotype. J Card Fail 15:529–539PubMed Miyamoto SD, Brown RD, Robinson BA, Tyler KL, Long CS, Debiasi RL (2009) Cardiac cell-specific apoptotic and cytokine responses to reovirus infection: determinants of myocarditic phenotype. J Card Fail 15:529–539PubMed
62.
go back to reference DeBiasi RL, Robinson BA, Leser JS, Brown RD, Long CS, Clarke P (2010) Critical role for death-receptor mediated apoptotic signaling in viral myocarditis. J Card Fail 16:901–910PubMed DeBiasi RL, Robinson BA, Leser JS, Brown RD, Long CS, Clarke P (2010) Critical role for death-receptor mediated apoptotic signaling in viral myocarditis. J Card Fail 16:901–910PubMed
63.
go back to reference Bowles NE, Ni J, Kearney DL, Pauschinger M, Schultheiss HP, McCarthy R, Hare J, Bricker JT, Bowles KR, Towbin JA (2003) Detection of viruses in myocardial tissues by polymerase chain reaction. Evidence of adenovirus as a common cause of myocarditis in children and adults. J Am Coll Cardiol 42:466–472PubMed Bowles NE, Ni J, Kearney DL, Pauschinger M, Schultheiss HP, McCarthy R, Hare J, Bricker JT, Bowles KR, Towbin JA (2003) Detection of viruses in myocardial tissues by polymerase chain reaction. Evidence of adenovirus as a common cause of myocarditis in children and adults. J Am Coll Cardiol 42:466–472PubMed
64.
go back to reference Blailock ZR, Rabin ER, Melnick JL (1968) Adenovirus myocarditis in mice. An electron microscopic study. Exp Mol Pathol 9:84–96PubMed Blailock ZR, Rabin ER, Melnick JL (1968) Adenovirus myocarditis in mice. An electron microscopic study. Exp Mol Pathol 9:84–96PubMed
65.
go back to reference Kajon AE, Brown CC, Spindler KR (1998) Distribution of mouse adenovirus type 1 in intraperitoneally and intranasally infected adult outbred mice. J Virol 72:1219–1223PubMed Kajon AE, Brown CC, Spindler KR (1998) Distribution of mouse adenovirus type 1 in intraperitoneally and intranasally infected adult outbred mice. J Virol 72:1219–1223PubMed
66.
go back to reference Guida JD, Fejer G, Pirofski LA, Brosnan CF, Horwitz MS (1995) Mouse adenovirus type 1 causes a fatal hemorrhagic encephalomyelitis in adult C57BL/6 but not BALB/c mice. J Virol 69:7674–7681PubMed Guida JD, Fejer G, Pirofski LA, Brosnan CF, Horwitz MS (1995) Mouse adenovirus type 1 causes a fatal hemorrhagic encephalomyelitis in adult C57BL/6 but not BALB/c mice. J Virol 69:7674–7681PubMed
67.
go back to reference Ashley SL, Welton AR, Harwood KM, Van Rooijen N, Spindler KR (2009) Mouse adenovirus type 1 infection of macrophages. Virology 390:307–314PubMed Ashley SL, Welton AR, Harwood KM, Van Rooijen N, Spindler KR (2009) Mouse adenovirus type 1 infection of macrophages. Virology 390:307–314PubMed
68.
go back to reference Nie X, Zhang G, Xu D, Sun X, Li Z, Li X, Zhang X, He F, Li Y (2010) The VP1-unique region of parvovirus B19 induces myocardial injury in mice. Scand J Infect Dis 42:121–128PubMed Nie X, Zhang G, Xu D, Sun X, Li Z, Li X, Zhang X, He F, Li Y (2010) The VP1-unique region of parvovirus B19 induces myocardial injury in mice. Scand J Infect Dis 42:121–128PubMed
69.
go back to reference Tzang BS, Lin TM, Tsai CC, Hsu JD, Yang LC, Hsu TC (2011) Increased cardiac injury in NZB/W F1 mice received antibody against human parvovirus B19 VP1 unique region protein. Mol Immunol 48:1518–1524PubMed Tzang BS, Lin TM, Tsai CC, Hsu JD, Yang LC, Hsu TC (2011) Increased cardiac injury in NZB/W F1 mice received antibody against human parvovirus B19 VP1 unique region protein. Mol Immunol 48:1518–1524PubMed
70.
go back to reference Hoelzer K, Parrish CR (2010) The emergence of parvoviruses of carnivores. Vet Res 41:39PubMed Hoelzer K, Parrish CR (2010) The emergence of parvoviruses of carnivores. Vet Res 41:39PubMed
71.
go back to reference Meurs KM, Fox PR, Magnon AL, Liu S, Towbin JA (2000) Molecular screening by polymerase chain reaction detects panleukopenia virus DNA in formalin-fixed hearts from cats with idiopathic cardiomyopathy and myocarditis. Cardiovasc Pathol 9:119–126PubMed Meurs KM, Fox PR, Magnon AL, Liu S, Towbin JA (2000) Molecular screening by polymerase chain reaction detects panleukopenia virus DNA in formalin-fixed hearts from cats with idiopathic cardiomyopathy and myocarditis. Cardiovasc Pathol 9:119–126PubMed
72.
go back to reference Agungpriyono DR, Uchida K, Tabaru H, Yamaguchi R, Tateyama S (1999) Subacute massive necrotizing myocarditis by canine parvovirus type 2 infection with diffuse leukoencephalomalacia in a puppy. Vet Pathol 36:77–80PubMed Agungpriyono DR, Uchida K, Tabaru H, Yamaguchi R, Tateyama S (1999) Subacute massive necrotizing myocarditis by canine parvovirus type 2 infection with diffuse leukoencephalomalacia in a puppy. Vet Pathol 36:77–80PubMed
73.
go back to reference Kawai C (1999) From myocarditis to cardiomyopathy: mechanisms of inflammation and cell death: learning from the past for the future. Circulation 99:1091–1100 (Review)PubMed Kawai C (1999) From myocarditis to cardiomyopathy: mechanisms of inflammation and cell death: learning from the past for the future. Circulation 99:1091–1100 (Review)PubMed
74.
go back to reference Häusler M, Sellhaus B, Scheithauer S, Gaida B, Kuropka S, Siepmann K, Panek A, Berg W, Teubner A, Ritter K, Kleines M (2007) Myocarditis in newborn wild-type BALB/c mice infected with the murine gamma herpesvirus MHV-68. Cardiovasc Res 76:323–330PubMed Häusler M, Sellhaus B, Scheithauer S, Gaida B, Kuropka S, Siepmann K, Panek A, Berg W, Teubner A, Ritter K, Kleines M (2007) Myocarditis in newborn wild-type BALB/c mice infected with the murine gamma herpesvirus MHV-68. Cardiovasc Res 76:323–330PubMed
75.
go back to reference Lenzo JC, Fairweather D, Cull V, Shellam GR, James Lawson CM (2002) Characterisation of murine cytomegalovirus myocarditis: cellular infiltration of the heart and virus persistence. J Mol Cell Cardiol 34:629–640PubMed Lenzo JC, Fairweather D, Cull V, Shellam GR, James Lawson CM (2002) Characterisation of murine cytomegalovirus myocarditis: cellular infiltration of the heart and virus persistence. J Mol Cell Cardiol 34:629–640PubMed
76.
go back to reference Ritter JT, Tang-Feldman YJ, Lochhead GR, Estrada M, Lochhead S, Yu C, Ashton-Sager A, Tuteja D, Leutenegger C, Pomeroy C (2010) In vivo characterization of cytokine profiles and viral load during murine cytomegalovirus-induced acute myocarditis. Cardiovasc Pathol 19:83–93PubMed Ritter JT, Tang-Feldman YJ, Lochhead GR, Estrada M, Lochhead S, Yu C, Ashton-Sager A, Tuteja D, Leutenegger C, Pomeroy C (2010) In vivo characterization of cytokine profiles and viral load during murine cytomegalovirus-induced acute myocarditis. Cardiovasc Pathol 19:83–93PubMed
77.
go back to reference Cull VS, Bartlett EJ, James CM (2002) Type I interferon gene therapy protects against cytomegalovirus-induced myocarditis. Immunology 106:428–437PubMed Cull VS, Bartlett EJ, James CM (2002) Type I interferon gene therapy protects against cytomegalovirus-induced myocarditis. Immunology 106:428–437PubMed
78.
go back to reference Mamas MA, Fraser D, Neyses L (2008) Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol 130:304–309PubMed Mamas MA, Fraser D, Neyses L (2008) Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol 130:304–309PubMed
79.
go back to reference Bratincsák A, El-Said HG, Bradley JS, Shayan K, Grossfeld PD, Cannavino CR (2010) Fulminant myocarditis associated with pandemic H1N1 influenza A virus in children. J Am Coll Cardiol 55:928–929PubMed Bratincsák A, El-Said HG, Bradley JS, Shayan K, Grossfeld PD, Cannavino CR (2010) Fulminant myocarditis associated with pandemic H1N1 influenza A virus in children. J Am Coll Cardiol 55:928–929PubMed
80.
go back to reference Pan HY, Yamada H, Chida J, Wang S, Yano M, Yao M, Zhu J, Kido H (2011) Up-regulation of ectopic trypsins in the myocardium by influenza A virus infection triggers acute myocarditis. Cardiovasc Res 89:595–603PubMed Pan HY, Yamada H, Chida J, Wang S, Yano M, Yao M, Zhu J, Kido H (2011) Up-regulation of ectopic trypsins in the myocardium by influenza A virus infection triggers acute myocarditis. Cardiovasc Res 89:595–603PubMed
81.
go back to reference Woo GH, Kim HY, Bae YC, Jean YH, Bak EJ, Kim MJ, Hwang EK, Joo YS (2011) Comparative histopathological characteristics of highly pathogenic avian influenza (HPAI) in chickens and domestic ducks in 2008 Korea. Histol Histopathol 26:167–175PubMed Woo GH, Kim HY, Bae YC, Jean YH, Bak EJ, Kim MJ, Hwang EK, Joo YS (2011) Comparative histopathological characteristics of highly pathogenic avian influenza (HPAI) in chickens and domestic ducks in 2008 Korea. Histol Histopathol 26:167–175PubMed
82.
go back to reference Gabriel G, Klingel K, Planz O, Bier K, Herwig A, Sauter M, Klenk HD (2009) Spread of infection and lymphocyte depletion in mice depends on polymerase of influenza virus. Am J Pathol 175:1178–1186PubMed Gabriel G, Klingel K, Planz O, Bier K, Herwig A, Sauter M, Klenk HD (2009) Spread of infection and lymphocyte depletion in mice depends on polymerase of influenza virus. Am J Pathol 175:1178–1186PubMed
83.
go back to reference Gabriel G, Klingel K, Otte A, Thiele S, Hudjetz B, Arman-Kalcek G, Sauter M, Shmidt T, Rother F, Baumgarte S, Keiner B, Hartmann E, Bader M, Brownlee GG, Fodor E, Klenk HD (2011) Differential use of importin-α isoforms governs cell tropism and host adaptation of influenza virus. Nat Commun 2:156PubMed Gabriel G, Klingel K, Otte A, Thiele S, Hudjetz B, Arman-Kalcek G, Sauter M, Shmidt T, Rother F, Baumgarte S, Keiner B, Hartmann E, Bader M, Brownlee GG, Fodor E, Klenk HD (2011) Differential use of importin-α isoforms governs cell tropism and host adaptation of influenza virus. Nat Commun 2:156PubMed
84.
go back to reference Durando MM, Birks EK, Hussey SB, Lunn DP (2011) Cardiac troponin I concentrations in ponies challenged with equine influenza virus. J Vet Intern Med 25:339–344PubMed Durando MM, Birks EK, Hussey SB, Lunn DP (2011) Cardiac troponin I concentrations in ponies challenged with equine influenza virus. J Vet Intern Med 25:339–344PubMed
85.
go back to reference Haugland O, Mikalsen AB, Nilsen P, Lindmo K, Thu BJ, Eliassen TM, Roos N, Rode M, Evensen O (2011) Cardiomyopathy syndrome of atlantic salmon (Salmo salar L.) is caused by a double-stranded RNA virus of the Totiviridae family. J Virol 85:5275–5286PubMed Haugland O, Mikalsen AB, Nilsen P, Lindmo K, Thu BJ, Eliassen TM, Roos N, Rode M, Evensen O (2011) Cardiomyopathy syndrome of atlantic salmon (Salmo salar L.) is caused by a double-stranded RNA virus of the Totiviridae family. J Virol 85:5275–5286PubMed
86.
go back to reference Fiedler A (1900) Über akute interstitielle Myokarditis. Zentralbl f Med 21:212–213 (Cited by Scott RW, Saphir O (1929–30) Acute isolated myocarditis. Am Heart J 5:129–141.) Fiedler A (1900) Über akute interstitielle Myokarditis. Zentralbl f Med 21:212–213 (Cited by Scott RW, Saphir O (1929–30) Acute isolated myocarditis. Am Heart J 5:129–141.)
87.
go back to reference Woodruff JF (1980) Viral Myocarditis. Am J Pathol 101:428–479 Woodruff JF (1980) Viral Myocarditis. Am J Pathol 101:428–479
88.
go back to reference Sainani GS, Dekate MP, Rao CP (1975) Heart disease caused by Coxsackie virus B infection. Br Heart J 37:819–823PubMed Sainani GS, Dekate MP, Rao CP (1975) Heart disease caused by Coxsackie virus B infection. Br Heart J 37:819–823PubMed
89.
go back to reference Gordon RB, Lennette EH, Sandrock RS (1959) The varied clinical manifestations of Coxsackie virus infections. Arch Int Med 103:63–75 Gordon RB, Lennette EH, Sandrock RS (1959) The varied clinical manifestations of Coxsackie virus infections. Arch Int Med 103:63–75
90.
go back to reference Null FC, Castle CH (1959) Adult pericarditis and myocarditis due to coxsackie virus, group B, type 5. N Engl J Med 26i:937–942 Null FC, Castle CH (1959) Adult pericarditis and myocarditis due to coxsackie virus, group B, type 5. N Engl J Med 26i:937–942
91.
go back to reference Smith WG (1970) Coxsackie B myocarditis in adults. Am Heart J 80:34–46PubMed Smith WG (1970) Coxsackie B myocarditis in adults. Am Heart J 80:34–46PubMed
92.
go back to reference Bell EJ, Grist NR (1970) Further studies of enterovirus infections in cardiac disease and pleurodynia. Scan J Infect Dis 2:1–6 Bell EJ, Grist NR (1970) Further studies of enterovirus infections in cardiac disease and pleurodynia. Scan J Infect Dis 2:1–6
93.
go back to reference Lerner AM, Wilson FM (1973) Virus myocardiomyopathy. Prog Med Virol 15:63–91PubMed Lerner AM, Wilson FM (1973) Virus myocardiomyopathy. Prog Med Virol 15:63–91PubMed
94.
go back to reference Medearis DN Jr (1957) Cytomegalic inclusion disease: an analysis of the clinical features based on the literature and 6 additional cases. Pediatrics 19:467–480PubMed Medearis DN Jr (1957) Cytomegalic inclusion disease: an analysis of the clinical features based on the literature and 6 additional cases. Pediatrics 19:467–480PubMed
95.
go back to reference Lenette DA, Specter S, Thompson KD (eds) (1979) Diagnosis of viral infections: The role of clinical laboratory. University Park Press, Baltimore Lenette DA, Specter S, Thompson KD (eds) (1979) Diagnosis of viral infections: The role of clinical laboratory. University Park Press, Baltimore
96.
go back to reference Grist NR, Reid D (1993) Epidemiology of viral infections of the heart. In: Banatvala JE (ed) Viral infections of the heart. Hodder and Stoughton, London, pp 23–31 Grist NR, Reid D (1993) Epidemiology of viral infections of the heart. In: Banatvala JE (ed) Viral infections of the heart. Hodder and Stoughton, London, pp 23–31
97.
go back to reference Mahfoud F, Gärtner B, Kindermann M, Ukena C, Gadomski K, Klingel K, Kandolf R, Böhm M, Kindermann I (2011) Virus serology in patients with suspected myocarditis: utility or futility? Eur Heart J 32:897–903PubMed Mahfoud F, Gärtner B, Kindermann M, Ukena C, Gadomski K, Klingel K, Kandolf R, Böhm M, Kindermann I (2011) Virus serology in patients with suspected myocarditis: utility or futility? Eur Heart J 32:897–903PubMed
98.
go back to reference Sakakibara S, Konno S (1962) Endomyocardial biopsy. Jpn Heart J 3:537–543PubMed Sakakibara S, Konno S (1962) Endomyocardial biopsy. Jpn Heart J 3:537–543PubMed
99.
go back to reference Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Ehrlich HA, Arnheim N (1985) Enzymatic amplification of β3-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354PubMed Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Ehrlich HA, Arnheim N (1985) Enzymatic amplification of β3-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350–1354PubMed
100.
go back to reference Pankuweit S, Portig I, Eckhardt H, Crombach M, Hufnagel G, Maisch B (2000) Prevalence of viral genome in endomyocardial biopsies from patients with inflammatory heart muscle disease. Herz 25(3):221–226PubMed Pankuweit S, Portig I, Eckhardt H, Crombach M, Hufnagel G, Maisch B (2000) Prevalence of viral genome in endomyocardial biopsies from patients with inflammatory heart muscle disease. Herz 25(3):221–226PubMed
101.
go back to reference Jackson DP, Lewis FA, Taylor GR, Boylston AW, Quirke P (1990) Tissue extraction of DNA and RNA and analysis by polymerase chain reaction. J Clin Pathol 43:499–504PubMed Jackson DP, Lewis FA, Taylor GR, Boylston AW, Quirke P (1990) Tissue extraction of DNA and RNA and analysis by polymerase chain reaction. J Clin Pathol 43:499–504PubMed
102.
go back to reference Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159PubMed Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159PubMed
103.
go back to reference Maniatis T, Fritsch EF, Sambrook J (1992) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor Maniatis T, Fritsch EF, Sambrook J (1992) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
104.
go back to reference Rotbart HA (1990) Enzymatic RNA amplification of enteroviruses. J Clin Microbiol 28:438–442PubMed Rotbart HA (1990) Enzymatic RNA amplification of enteroviruses. J Clin Microbiol 28:438–442PubMed
105.
go back to reference Martin AB, Webber S, Fricker J, Jaffe R et al (1994) Acute myocarditis: rapid diagnosis in children. Circulation 90:330–339PubMed Martin AB, Webber S, Fricker J, Jaffe R et al (1994) Acute myocarditis: rapid diagnosis in children. Circulation 90:330–339PubMed
106.
go back to reference Kandolf R, Ameis D, Kirschner P, Canu A, Hofschneider PH (1987) In situ detection of enteroviral genomes in myocardial cells by nucleic acid hybridization: an approach to the diagnosis of viral heart disease. Proc Natl Acad Sci USA 84:6272–6276PubMed Kandolf R, Ameis D, Kirschner P, Canu A, Hofschneider PH (1987) In situ detection of enteroviral genomes in myocardial cells by nucleic acid hybridization: an approach to the diagnosis of viral heart disease. Proc Natl Acad Sci USA 84:6272–6276PubMed
107.
go back to reference Klingel K, Stephan S, Sauter M, Zell R et al (1996) Pathogenesis of murine enterovirus myocarditis: virus dissemination and immune target cells. J Virol 70:8888–8895PubMed Klingel K, Stephan S, Sauter M, Zell R et al (1996) Pathogenesis of murine enterovirus myocarditis: virus dissemination and immune target cells. J Virol 70:8888–8895PubMed
108.
go back to reference Klump WM, Bergmann I, Müller BC, Ameis D, Kandolf R (1990) Complete nucleotide sequence of infectious coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J Virol 64:1573–1583PubMed Klump WM, Bergmann I, Müller BC, Ameis D, Kandolf R (1990) Complete nucleotide sequence of infectious coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J Virol 64:1573–1583PubMed
109.
go back to reference Archard L, Khan M, Soteriou BA et al (1997) Characterisation of coxsackie B virus RNA in myocardium from patients with dilated cardiomyopathy by nucleotide sequencing of reverse transcription-nested polymerase chain reaction products. Hum Pathol 29:578–584 Archard L, Khan M, Soteriou BA et al (1997) Characterisation of coxsackie B virus RNA in myocardium from patients with dilated cardiomyopathy by nucleotide sequencing of reverse transcription-nested polymerase chain reaction products. Hum Pathol 29:578–584
110.
go back to reference Chapman NM, Tracy S, Gauntt CJ, Fortmüller U (1990) Molecular detection and identification of enteroviruses using enzymatic amplification and nucleic acid hybridisation. J Clin Microbiol 28:843–850PubMed Chapman NM, Tracy S, Gauntt CJ, Fortmüller U (1990) Molecular detection and identification of enteroviruses using enzymatic amplification and nucleic acid hybridisation. J Clin Microbiol 28:843–850PubMed
111.
go back to reference Grasso M, Arbustini E, Silini E et al (1992) Search for Coxsackievirus B3 RNA in idiopathic dilated cardiomyopathy using gene amplification by polymerase chain reaction. Am J Cardiol 69:658–664PubMed Grasso M, Arbustini E, Silini E et al (1992) Search for Coxsackievirus B3 RNA in idiopathic dilated cardiomyopathy using gene amplification by polymerase chain reaction. Am J Cardiol 69:658–664PubMed
112.
go back to reference Tracy S, Chapman NM, McManus BM et al (1990) A molecular and serologic evaluation of enteroviral involvement in human myocarditis. J Mol Cell Cardiol 22:403–414PubMed Tracy S, Chapman NM, McManus BM et al (1990) A molecular and serologic evaluation of enteroviral involvement in human myocarditis. J Mol Cell Cardiol 22:403–414PubMed
113.
go back to reference Schowengerdt K, Ni J, Denfield S et al (1997) Association of parvovirus B19 genome in children with myocarditis and cardiac allograft rejection. Diagnosis using the polymerase chain reaction. Circulation 96:3549–3554PubMed Schowengerdt K, Ni J, Denfield S et al (1997) Association of parvovirus B19 genome in children with myocarditis and cardiac allograft rejection. Diagnosis using the polymerase chain reaction. Circulation 96:3549–3554PubMed
114.
go back to reference Piiparinen H, Vaheri A (1991) Genotyping of herpes simplex viruses by polymerase chain reaction. Arch Virol 119:541–548 Piiparinen H, Vaheri A (1991) Genotyping of herpes simplex viruses by polymerase chain reaction. Arch Virol 119:541–548
115.
go back to reference Weiss SM, Roblin PM, Gaydos CA et al (1996) Failure to detect chlamydia pneumoniae in coronary atheromas of patients undergoing atherectomy. J Infect Dis 173:957–962PubMed Weiss SM, Roblin PM, Gaydos CA et al (1996) Failure to detect chlamydia pneumoniae in coronary atheromas of patients undergoing atherectomy. J Infect Dis 173:957–962PubMed
116.
go back to reference Goodman JL, Jurkovic P, Kramber JM, Johnson RC (1991) Molecular detection of persistent borrelia burgdorferi in the urine of patients with active Lyme disease. Infect Immunol 59:269–278 Goodman JL, Jurkovic P, Kramber JM, Johnson RC (1991) Molecular detection of persistent borrelia burgdorferi in the urine of patients with active Lyme disease. Infect Immunol 59:269–278
117.
go back to reference Stanek G, Klein J, Bitnner R, Glogar D (1990) Isolation of borrelia burgdorferi from the myocardium of a patient with longstanding cardiomyopathy. N Engl J Med 322:249–252PubMed Stanek G, Klein J, Bitnner R, Glogar D (1990) Isolation of borrelia burgdorferi from the myocardium of a patient with longstanding cardiomyopathy. N Engl J Med 322:249–252PubMed
118.
go back to reference Nakhleh RE, Copenhaver CM, Werdin K (1991) Lack of evidence for involvment of Epstein-Barr virus in the development of ‘Quilty’ lesion of transplanted hearts: an in situ hybridization study. J Heart Lung Transpl 10:504–507 Nakhleh RE, Copenhaver CM, Werdin K (1991) Lack of evidence for involvment of Epstein-Barr virus in the development of ‘Quilty’ lesion of transplanted hearts: an in situ hybridization study. J Heart Lung Transpl 10:504–507
119.
go back to reference Klingel K, Sauter M, Bock CT, Szalay G, Schnorr JJ, Kandolf R (2004) Molecular pathology of inflammatory cardiomyopathy. Med Microbiol Immunol (Berl) 193(2–3):101–107 Klingel K, Sauter M, Bock CT, Szalay G, Schnorr JJ, Kandolf R (2004) Molecular pathology of inflammatory cardiomyopathy. Med Microbiol Immunol (Berl) 193(2–3):101–107
120.
go back to reference Kandolf R, Hofschneider PH (1985) Molecular cloning of the genome of a cardiotropic coxsackie B3 virus: full-length reverse-transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc Natl Acad Sci USA 82:4818–4822PubMed Kandolf R, Hofschneider PH (1985) Molecular cloning of the genome of a cardiotropic coxsackie B3 virus: full-length reverse-transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc Natl Acad Sci USA 82:4818–4822PubMed
121.
go back to reference Manaresi E, Gallinella G, Zuffi E, Bonvicini F, Zerbini M, Musiani M (2002) Diagnosis and quantitative evaluation of parvovirus B19 infections by real-time PCR in the clinical laboratory. J Med Virol 67:275–281PubMed Manaresi E, Gallinella G, Zuffi E, Bonvicini F, Zerbini M, Musiani M (2002) Diagnosis and quantitative evaluation of parvovirus B19 infections by real-time PCR in the clinical laboratory. J Med Virol 67:275–281PubMed
122.
go back to reference Harder TC, Hufnagel M, Zahn K, Beutel K, Schmitt H-J, Ullmann U et al (2001) New LightCycler PCR for rapid and sensitive quantification of parvovirus B19 DNA guides therapeutic decision-making in relapsing infections. J Clin Microbiol 39:4413–4419PubMed Harder TC, Hufnagel M, Zahn K, Beutel K, Schmitt H-J, Ullmann U et al (2001) New LightCycler PCR for rapid and sensitive quantification of parvovirus B19 DNA guides therapeutic decision-making in relapsing infections. J Clin Microbiol 39:4413–4419PubMed
123.
go back to reference Aberham C, Pendl C, Gross P, Zerlauth G, Gessner M (2001) A quantitative, internally controlled real-time PCR Assay for the detection of parvovirus B19 DNA. J Virol Methods 92:183–191PubMed Aberham C, Pendl C, Gross P, Zerlauth G, Gessner M (2001) A quantitative, internally controlled real-time PCR Assay for the detection of parvovirus B19 DNA. J Virol Methods 92:183–191PubMed
124.
go back to reference Gruber F, Falkner FG, Dorner F, Hammerle T (2001) Quantitation of viral DNA by real-time PCR applying duplex amplification, internal standardization, and two-color fluorescence detection. Appl Environ Microbiol 67:2837–2839PubMed Gruber F, Falkner FG, Dorner F, Hammerle T (2001) Quantitation of viral DNA by real-time PCR applying duplex amplification, internal standardization, and two-color fluorescence detection. Appl Environ Microbiol 67:2837–2839PubMed
125.
go back to reference Servant A, Laperche S, Lallemand F, Marinho V, De Maur G, Meritet JF, Garbarg-Chenon A (2002) Genetic diversity within human erythroviruses: identification of three genotypes. J Virol 76:9124–9134PubMed Servant A, Laperche S, Lallemand F, Marinho V, De Maur G, Meritet JF, Garbarg-Chenon A (2002) Genetic diversity within human erythroviruses: identification of three genotypes. J Virol 76:9124–9134PubMed
126.
go back to reference Hokynar K, Soderlund-Venermo M, Pesonen M, Ranki A, Kiviluoto O, Partio EK, Hedman K (2002) A new parvovirus genotype persistent in human skin. Virology 302:224–228PubMed Hokynar K, Soderlund-Venermo M, Pesonen M, Ranki A, Kiviluoto O, Partio EK, Hedman K (2002) A new parvovirus genotype persistent in human skin. Virology 302:224–228PubMed
127.
go back to reference Nguyen QT, WongS HeegaardED, Brown KE (2002) Identification and characterization of a second novel human erythrovirus variant A6. Virology 301:374–380PubMed Nguyen QT, WongS HeegaardED, Brown KE (2002) Identification and characterization of a second novel human erythrovirus variant A6. Virology 301:374–380PubMed
128.
go back to reference Heegaard ED, Brown KE (2002) Human parvovirus B 19. Clin Microbiol Rev 15:485–505PubMed Heegaard ED, Brown KE (2002) Human parvovirus B 19. Clin Microbiol Rev 15:485–505PubMed
129.
go back to reference Liefeldt L, Plentz A, Klempa B, Kershaw O, Endres AS, Raab U, Neumayer HH, Meisel H, Modrow S (2005) Recurrent high level parvovirus B19/genotype 2 viremia in a renal transplant recipient analyzed by real-time PCR for simultaneous detection of genotypes 1 to 3. J Med Virol 75(1):161–169PubMed Liefeldt L, Plentz A, Klempa B, Kershaw O, Endres AS, Raab U, Neumayer HH, Meisel H, Modrow S (2005) Recurrent high level parvovirus B19/genotype 2 viremia in a renal transplant recipient analyzed by real-time PCR for simultaneous detection of genotypes 1 to 3. J Med Virol 75(1):161–169PubMed
130.
go back to reference Yajima T, Knowlton KU (2009) Viral myocarditis: from the perspective of the virus. Circulation 119:2615–2624PubMed Yajima T, Knowlton KU (2009) Viral myocarditis: from the perspective of the virus. Circulation 119:2615–2624PubMed
131.
go back to reference Bowles NE, Rose ML, Taylor P et al (1989) End-stage dilated cardiomyopathy persistence of enterovirus RNA in myocardium at cardiac transplantation and lack of immune response. Circulation 80:1128–1136PubMed Bowles NE, Rose ML, Taylor P et al (1989) End-stage dilated cardiomyopathy persistence of enterovirus RNA in myocardium at cardiac transplantation and lack of immune response. Circulation 80:1128–1136PubMed
132.
go back to reference Tracy S, Wiegand V, McManus B et al (1990) Molecular approaches to enteroviral diagnosis in idiopathic cardiomyopathy and myocarditis. JACC 15:1688–1694PubMed Tracy S, Wiegand V, McManus B et al (1990) Molecular approaches to enteroviral diagnosis in idiopathic cardiomyopathy and myocarditis. JACC 15:1688–1694PubMed
133.
go back to reference Jin O, Sole M, Butany JW et al (1990) Detection of enterovirus RNA in myocardial biopsies from patients with myocarditis and cardiomyopathy using gene amplification by polymerase chain reaction. Circulation 82:8–16PubMed Jin O, Sole M, Butany JW et al (1990) Detection of enterovirus RNA in myocardial biopsies from patients with myocarditis and cardiomyopathy using gene amplification by polymerase chain reaction. Circulation 82:8–16PubMed
134.
go back to reference Weiss L, Mohaved L, Billingham ME, Cleary ML (1991) Detection of coxsackie B3 RNA in myocardial tissues by polymerase chain reaction. Am J Pathol 138:497–503PubMed Weiss L, Mohaved L, Billingham ME, Cleary ML (1991) Detection of coxsackie B3 RNA in myocardial tissues by polymerase chain reaction. Am J Pathol 138:497–503PubMed
135.
go back to reference Kandolf R, Klingel K, Zell R et al (1993) Molecular pathogenesis of enterovirus-induced myocarditis: virus persistence and chronic inflammation. Intervirology 35:140–150PubMed Kandolf R, Klingel K, Zell R et al (1993) Molecular pathogenesis of enterovirus-induced myocarditis: virus persistence and chronic inflammation. Intervirology 35:140–150PubMed
136.
go back to reference Petitjan J, Kopecka H, Freymuth F et al (1992) Detection of enteroviruses in endomyocardial biopsy by molecular approach. J Med Virol 37:76–82 Petitjan J, Kopecka H, Freymuth F et al (1992) Detection of enteroviruses in endomyocardial biopsy by molecular approach. J Med Virol 37:76–82
137.
go back to reference Pauschinger M, Dörner G, Meissner G et al (1994) Enteroviral RNA detection by polymerase chain reaction (PCR) in cardiac muscle biopsies of patients with myocarditis or dilated cardiomyopathy. J Am Coll Cardiol 2:880–884 Pauschinger M, Dörner G, Meissner G et al (1994) Enteroviral RNA detection by polymerase chain reaction (PCR) in cardiac muscle biopsies of patients with myocarditis or dilated cardiomyopathy. J Am Coll Cardiol 2:880–884
138.
go back to reference Bowles N, Towbin J (1996) Viral heart muscle disease in children. Newslett Sci Counc Cardiomyopathies 11:4–5 Bowles N, Towbin J (1996) Viral heart muscle disease in children. Newslett Sci Counc Cardiomyopathies 11:4–5
139.
go back to reference Talwar KK, Thatai D, Kannath P et al (1996) Enteroviral detection by polymerase chain reaction technique in endomyocardial biopsy specimen: an initial study. Indian Heart J 48:479–480 Talwar KK, Thatai D, Kannath P et al (1996) Enteroviral detection by polymerase chain reaction technique in endomyocardial biopsy specimen: an initial study. Indian Heart J 48:479–480
140.
go back to reference Maisch B, Schönian U, Hufnagel G, Pankuweit S (1997) Enteroviral persistence in myocarditis and dilated cardiomyopathy. Eur Heart J 18:593 Maisch B, Schönian U, Hufnagel G, Pankuweit S (1997) Enteroviral persistence in myocarditis and dilated cardiomyopathy. Eur Heart J 18:593
141.
go back to reference Pauschinger M, Phan MD, Dörner A et al (1997) Detection of enteroviral RNA replicative intermediates in endomyocardial biopsies: indication of viral replication in the human heart. Eur Heart J 18:594A Pauschinger M, Phan MD, Dörner A et al (1997) Detection of enteroviral RNA replicative intermediates in endomyocardial biopsies: indication of viral replication in the human heart. Eur Heart J 18:594A
142.
go back to reference Kuhl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, Poller W, Kandolf R, Schultheiss HP (2005) High prevalence of viral genomes and multiple viral infections in the myocardium of adults with idiopathic left ventricular dysfunction. Circulation 111:887–893PubMed Kuhl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, Poller W, Kandolf R, Schultheiss HP (2005) High prevalence of viral genomes and multiple viral infections in the myocardium of adults with idiopathic left ventricular dysfunction. Circulation 111:887–893PubMed
143.
go back to reference Pankuweit S, Ruppert V, Eckhardt H, Strache D, Maisch B (2005) Pathophysiology and etiological diagnosis of inflammatory myocardial diseases with a special focus on parvovirus B 19. J Vet Med B Infect Dis Vet Public Health 52(7–8):344–347PubMed Pankuweit S, Ruppert V, Eckhardt H, Strache D, Maisch B (2005) Pathophysiology and etiological diagnosis of inflammatory myocardial diseases with a special focus on parvovirus B 19. J Vet Med B Infect Dis Vet Public Health 52(7–8):344–347PubMed
144.
go back to reference Mahrholdt H, Wagner A, Deluigi CC, Kispert E, Hager S, Meinhardt G, Vogelsberg H, Fritz P, Dippon J, Bock CT, Klingel K, Kandolf R, Sechtem U (2006) Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 114(15):1581–1590PubMed Mahrholdt H, Wagner A, Deluigi CC, Kispert E, Hager S, Meinhardt G, Vogelsberg H, Fritz P, Dippon J, Bock CT, Klingel K, Kandolf R, Sechtem U (2006) Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 114(15):1581–1590PubMed
145.
go back to reference Kandolf R, Bültmann B, Klingel K, Bock CT (2008) Molecular mechanisms and consequences of cardiac viral infections. Pathologe 29(Suppl 2):112–117PubMed Kandolf R, Bültmann B, Klingel K, Bock CT (2008) Molecular mechanisms and consequences of cardiac viral infections. Pathologe 29(Suppl 2):112–117PubMed
146.
go back to reference Pauschinger M, Dörner A, Kühl U et al (1999) Enteroviral replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 99:889–895PubMed Pauschinger M, Dörner A, Kühl U et al (1999) Enteroviral replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 99:889–895PubMed
147.
go back to reference Chapman M, Kim KS (2008) Persistent coxsackievirus infection: enterovirus persistence in chronic myocarditis and dilated cardiomyopathy. Curr Top Microbiol Immunol 323:275–292PubMed Chapman M, Kim KS (2008) Persistent coxsackievirus infection: enterovirus persistence in chronic myocarditis and dilated cardiomyopathy. Curr Top Microbiol Immunol 323:275–292PubMed
148.
go back to reference Kytö V, Vuorinen T, Saukko P, Lautenschlager I, Lignitz E, Saraste A, Voipio-Pulkki LM (2005) Cytomegalovirus infection of the heart is common in patients with fatal myocarditis. Clin Infect Dis 40(5):683–688PubMed Kytö V, Vuorinen T, Saukko P, Lautenschlager I, Lignitz E, Saraste A, Voipio-Pulkki LM (2005) Cytomegalovirus infection of the heart is common in patients with fatal myocarditis. Clin Infect Dis 40(5):683–688PubMed
149.
go back to reference Maisch B, Schönian U, Crombach M et al (1993) Cytomegalovirus associated inflammatory heart muscle disease. Scan J Infect Dis suppl 88:135–148 Maisch B, Schönian U, Crombach M et al (1993) Cytomegalovirus associated inflammatory heart muscle disease. Scan J Infect Dis suppl 88:135–148
150.
go back to reference Schönian U, Crombach M, Maisch B (1993) Assessment of cytomegalovirus DNA and protein expression in patients with myocarditis. Clin Immun Immunpathol 68:229–233 Schönian U, Crombach M, Maisch B (1993) Assessment of cytomegalovirus DNA and protein expression in patients with myocarditis. Clin Immun Immunpathol 68:229–233
151.
go back to reference Towbin JA (1996) Diagnosis and management of myocarditis in children. Newsletter of the Scientific Council on Cardiomyopathies 11:8 Towbin JA (1996) Diagnosis and management of myocarditis in children. Newsletter of the Scientific Council on Cardiomyopathies 11:8
152.
go back to reference Maisch B, Pausch R, Hufnagel G, Schönian U (1997) The neglected role of DNA viruses in chronic myocarditis and dilated cardiomyopathy. Eur Heart J 18:515 Maisch B, Pausch R, Hufnagel G, Schönian U (1997) The neglected role of DNA viruses in chronic myocarditis and dilated cardiomyopathy. Eur Heart J 18:515
153.
go back to reference Bergelson JM, Cunningham JA, Droguett G et al (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323PubMed Bergelson JM, Cunningham JA, Droguett G et al (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323PubMed
154.
go back to reference Tomko RP, Xu R, Philipson L (1997) HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci USA 94:3352–3356PubMed Tomko RP, Xu R, Philipson L (1997) HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci USA 94:3352–3356PubMed
155.
go back to reference Hufnagel G, Busse C, Ische B, Maisch B (1997) Detection of adenoviral DNA in endomyocardial biopsies of adult patients with myocarditis and dilated cardiomyopathy. Eur Heart J 18:515 Hufnagel G, Busse C, Ische B, Maisch B (1997) Detection of adenoviral DNA in endomyocardial biopsies of adult patients with myocarditis and dilated cardiomyopathy. Eur Heart J 18:515
156.
go back to reference Pauschinger M, Bowles NE, Fuentes-Garcia FJ et al (1999) Detection of adenoviral genome in the myocardium of adult patients with idiopathic left ventricular dysfunction. Circulation 99:1348–1354PubMed Pauschinger M, Bowles NE, Fuentes-Garcia FJ et al (1999) Detection of adenoviral genome in the myocardium of adult patients with idiopathic left ventricular dysfunction. Circulation 99:1348–1354PubMed
157.
go back to reference Rohayem J, Dinger J, Fischer R et al (2001) Fatal myocarditis associated with acute parvovirus B19 and human herpesvirus 6 coinfection. J Clin Microbiol 39:4585–4587PubMed Rohayem J, Dinger J, Fischer R et al (2001) Fatal myocarditis associated with acute parvovirus B19 and human herpesvirus 6 coinfection. J Clin Microbiol 39:4585–4587PubMed
158.
go back to reference Heegaard ED, Eiskjaer H, Baandrup U et al (1998) Case report: parvovirus B19 infection associated with myocarditis following adult cardiac transplantation. Scand J Infect Dis 30:607–610PubMed Heegaard ED, Eiskjaer H, Baandrup U et al (1998) Case report: parvovirus B19 infection associated with myocarditis following adult cardiac transplantation. Scand J Infect Dis 30:607–610PubMed
159.
go back to reference Chia JKS (1996) Myopericarditis due to parvovirus B19 in an adult. Clin Infect Dis 23:200–201PubMed Chia JKS (1996) Myopericarditis due to parvovirus B19 in an adult. Clin Infect Dis 23:200–201PubMed
160.
go back to reference Schwarz TF, Wiersbitzky S, Pambor M (1994) Case report: detection of parvovirus B19 in a skin biopsy of a patient with erythema infectiosum. J Med Virol 43:171–174PubMed Schwarz TF, Wiersbitzky S, Pambor M (1994) Case report: detection of parvovirus B19 in a skin biopsy of a patient with erythema infectiosum. J Med Virol 43:171–174PubMed
161.
go back to reference Gabriel SE, Espy M, Erdman DD et al (1999) The role of parvovirus B19 in the pathogenesis of giant cell arteritis. Arthritis Rheum 42:1255–1258PubMed Gabriel SE, Espy M, Erdman DD et al (1999) The role of parvovirus B19 in the pathogenesis of giant cell arteritis. Arthritis Rheum 42:1255–1258PubMed
162.
go back to reference Nigro G, Bastianon V, Colloridi V et al (2000) Human parvovirus B19 infection in infancy associated with acute and chronic lymphocytic myocarditis and high cytokine levels: report of 3 cases and review. Clin Infect Dis 31:65–69PubMed Nigro G, Bastianon V, Colloridi V et al (2000) Human parvovirus B19 infection in infancy associated with acute and chronic lymphocytic myocarditis and high cytokine levels: report of 3 cases and review. Clin Infect Dis 31:65–69PubMed
163.
go back to reference Sokal EM, Melchior M, Cornu C et al (1998) Acute parvovirus B19 infection associated with fulminant hepatitis of favourable prognosis in young children. Lancet 352:1739–1741PubMed Sokal EM, Melchior M, Cornu C et al (1998) Acute parvovirus B19 infection associated with fulminant hepatitis of favourable prognosis in young children. Lancet 352:1739–1741PubMed
164.
go back to reference Enders M, Klingel K, Weidner A, Baisch C, Kandolf R, Schalasta G, Enders G (2010) Risk of fetal hydrops and non-hydropic late intrauterine fetal death after gestational parvovirus B19 infection. J Clin Virol 49:163–168PubMed Enders M, Klingel K, Weidner A, Baisch C, Kandolf R, Schalasta G, Enders G (2010) Risk of fetal hydrops and non-hydropic late intrauterine fetal death after gestational parvovirus B19 infection. J Clin Virol 49:163–168PubMed
165.
go back to reference Brown KE, Anderson SM, Young NS (1993) Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114–117PubMed Brown KE, Anderson SM, Young NS (1993) Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114–117PubMed
166.
go back to reference Porter HJ, Quantrill AM, Fleming KA (1998) B19 parvovirus infection of myocardial cells. Lancet 1:535–536 Porter HJ, Quantrill AM, Fleming KA (1998) B19 parvovirus infection of myocardial cells. Lancet 1:535–536
167.
go back to reference Pankuweit S, Moll R, Baantrup U, Portig I, Hufnagel G, Maisch B (2003) Prevalence of the parvovirus B19 genome in endomyocardial biopsy specimens. Hum Pathol 34:497–500PubMed Pankuweit S, Moll R, Baantrup U, Portig I, Hufnagel G, Maisch B (2003) Prevalence of the parvovirus B19 genome in endomyocardial biopsy specimens. Hum Pathol 34:497–500PubMed
168.
go back to reference Klein RM, Jiang H, Niederacher D, Adams O, Du M, Horlitz M, Schley P, Marx R, Lankisch MR, Brehm MU, Strauer BE, Gabbert HE, Scheffold T, Gülker H (2004) Frequency and quantity of the parvovirus B19 genome in endomyocardial biopsies from patients with suspected myocarditis or idiopathic left ventricular dysfunction. Z Kardiol 93(4):300–309PubMed Klein RM, Jiang H, Niederacher D, Adams O, Du M, Horlitz M, Schley P, Marx R, Lankisch MR, Brehm MU, Strauer BE, Gabbert HE, Scheffold T, Gülker H (2004) Frequency and quantity of the parvovirus B19 genome in endomyocardial biopsies from patients with suspected myocarditis or idiopathic left ventricular dysfunction. Z Kardiol 93(4):300–309PubMed
169.
go back to reference Kühl U, Pauschinger M, Bock T, Klingel K, Schwimmbeck CP, Seeberg B, Krautwurm L, Poller W, Schultheiss HP, Kandolf R (2003) Parvovirus B19 infection mimicking acute myocardial infarction. Circulation 108(8):945–950PubMed Kühl U, Pauschinger M, Bock T, Klingel K, Schwimmbeck CP, Seeberg B, Krautwurm L, Poller W, Schultheiss HP, Kandolf R (2003) Parvovirus B19 infection mimicking acute myocardial infarction. Circulation 108(8):945–950PubMed
170.
go back to reference Bültmann BD, Klingel K, Sotlar K, Bock CT, Baba HA, Sauter M, Kandolf R (2003) Fatal parvovirus B19-associated myocarditis clinically mimicking ischemic heart disease: an endothelial cell-mediated disease. Hum Pathol 34:92–95PubMed Bültmann BD, Klingel K, Sotlar K, Bock CT, Baba HA, Sauter M, Kandolf R (2003) Fatal parvovirus B19-associated myocarditis clinically mimicking ischemic heart disease: an endothelial cell-mediated disease. Hum Pathol 34:92–95PubMed
171.
go back to reference Kuethe F, Lindner J, Matschke K, Wenzel JJ, Norja P, Ploetze K, Schaal S, Kamvissi V, Bornstein SR, Schwanebeck U, Modrow S (2009) Prevalence of parvovirus B19 and human bocavirus DNA in the heart of patients with no evidence of dilated cardiomyopathy or myocarditis. Clin Infect Dis 49:1660–1666PubMed Kuethe F, Lindner J, Matschke K, Wenzel JJ, Norja P, Ploetze K, Schaal S, Kamvissi V, Bornstein SR, Schwanebeck U, Modrow S (2009) Prevalence of parvovirus B19 and human bocavirus DNA in the heart of patients with no evidence of dilated cardiomyopathy or myocarditis. Clin Infect Dis 49:1660–1666PubMed
172.
go back to reference Lotze U, Egerer R, Glück B, Zell R, Sigusch H, Erhardt C, Heim A, Kandolf R, Bock T, Wutzler P, Figulla HR (2010) Low level myocardial parvovirus B19 persistence is a frequent finding in patients with heart disease but unrelated to ongoing myocardial injury. J Med Virol 82:1449–1457PubMed Lotze U, Egerer R, Glück B, Zell R, Sigusch H, Erhardt C, Heim A, Kandolf R, Bock T, Wutzler P, Figulla HR (2010) Low level myocardial parvovirus B19 persistence is a frequent finding in patients with heart disease but unrelated to ongoing myocardial injury. J Med Virol 82:1449–1457PubMed
173.
go back to reference Corcioli F, Zakrzewska K, Rinieri A, Fanci R, Innocenti M, Civinini R, De Giorgi V, Di Lollo S, Azzi A (2008) Tissue persistence of parvovirus B19 genotypes in asymptomatic persons. J Med Virol 80:2005–2011PubMed Corcioli F, Zakrzewska K, Rinieri A, Fanci R, Innocenti M, Civinini R, De Giorgi V, Di Lollo S, Azzi A (2008) Tissue persistence of parvovirus B19 genotypes in asymptomatic persons. J Med Virol 80:2005–2011PubMed
174.
go back to reference Schenk T, Enders M, Pollak S, Hahn R, Huzly D (2009) High prevalence of human parvovirus B19 DNA in myocardial autopsy samples from subjects without myocarditis or dilative cardiomyopathy. J Clin Microbiol 47:106–110PubMed Schenk T, Enders M, Pollak S, Hahn R, Huzly D (2009) High prevalence of human parvovirus B19 DNA in myocardial autopsy samples from subjects without myocarditis or dilative cardiomyopathy. J Clin Microbiol 47:106–110PubMed
175.
go back to reference Stewart GC, Lopez-Molina J, Gottumukkala RV, Rosner GF, Anello MS, Hecht JL, Winters GL, Padera RF, Baughman KL, Lipes MA (2011) Myocardial parvovirus B19 persistence: lack of association with clinicopathologic phenotype in adults with heart failure. Circ Heart Fail 4(1):71–78PubMed Stewart GC, Lopez-Molina J, Gottumukkala RV, Rosner GF, Anello MS, Hecht JL, Winters GL, Padera RF, Baughman KL, Lipes MA (2011) Myocardial parvovirus B19 persistence: lack of association with clinicopathologic phenotype in adults with heart failure. Circ Heart Fail 4(1):71–78PubMed
176.
go back to reference Schmidt-Lucke C, Spillmann F, Bock T, Kühl U, Van Linthout S, Schultheiss HP, Tschöpe C (2010) Interferon beta modulates endothelial damage in patients with cardiac persistence of human parvovirus b19 infection. J Infect Dis 201:936–945PubMed Schmidt-Lucke C, Spillmann F, Bock T, Kühl U, Van Linthout S, Schultheiss HP, Tschöpe C (2010) Interferon beta modulates endothelial damage in patients with cardiac persistence of human parvovirus b19 infection. J Infect Dis 201:936–945PubMed
177.
go back to reference Zafrir B, Aviv A, Reichman N, Flatau E (2005) Epstein-Barr virus associated pericarditis and pericardial effusion: case report and diagnostic aspects. Eur J Intern Med 16:528–530PubMed Zafrir B, Aviv A, Reichman N, Flatau E (2005) Epstein-Barr virus associated pericarditis and pericardial effusion: case report and diagnostic aspects. Eur J Intern Med 16:528–530PubMed
178.
go back to reference Roubille F, Gahide G, Moore-Morris T, Granier M, Davy JM, Vernhet H, Piot C (2008) Epstein Barr virus (EBV) and acute myopericarditis in an immunocompetent patient: first demonstrated case and discussion. Intern Med 47(7):627–629PubMed Roubille F, Gahide G, Moore-Morris T, Granier M, Davy JM, Vernhet H, Piot C (2008) Epstein Barr virus (EBV) and acute myopericarditis in an immunocompetent patient: first demonstrated case and discussion. Intern Med 47(7):627–629PubMed
179.
go back to reference Chang YL, Parker ME, Nuovo G, Miller JB (2009) Human herpesvirus 6–related fulminant myocarditis and hepatitis in an immunocompetent adult with fatal outcome. Hum Pathol 40(5):740–745PubMed Chang YL, Parker ME, Nuovo G, Miller JB (2009) Human herpesvirus 6–related fulminant myocarditis and hepatitis in an immunocompetent adult with fatal outcome. Hum Pathol 40(5):740–745PubMed
180.
go back to reference Leveque N, Boulagnon C, Brasselet C, Lesaffre F, Boutolleau D, Metz D, Fornes P, Andreoletti L (2011) A fatal case of Human Herpesvirus 6 chronic myocarditis in an immunocompetent adult. J Clin Virol 52(2):142–145PubMed Leveque N, Boulagnon C, Brasselet C, Lesaffre F, Boutolleau D, Metz D, Fornes P, Andreoletti L (2011) A fatal case of Human Herpesvirus 6 chronic myocarditis in an immunocompetent adult. J Clin Virol 52(2):142–145PubMed
181.
go back to reference Liao YC, Hsieh YC, Chang WC, Huang JL, Ting CT, Wu TJ (2011) Fulminant myocarditis in an adult with 2009 pandemic influenza A (H1N1 influenza) infection. J Chin Med Assoc 74(3):130–133PubMed Liao YC, Hsieh YC, Chang WC, Huang JL, Ting CT, Wu TJ (2011) Fulminant myocarditis in an adult with 2009 pandemic influenza A (H1N1 influenza) infection. J Chin Med Assoc 74(3):130–133PubMed
182.
go back to reference Moulik M, Breinholt JP, Dreyer WJ, Kearney DL, Price JF, Clunie SK, Moffett BS, Kim JJ, Rossano JW, Jefferies JL, Bowles KR, O’Brian Smith E, Bowles NE, Denfield SW, Towbin JA (2010) Viral endomyocardial infection is an independent predictor and potentially treatable risk factor for graft loss and coronary vasculopathy in pediatric cardiac transplant recipients. J Am Coll Cardiol 56(7):582–592PubMed Moulik M, Breinholt JP, Dreyer WJ, Kearney DL, Price JF, Clunie SK, Moffett BS, Kim JJ, Rossano JW, Jefferies JL, Bowles KR, O’Brian Smith E, Bowles NE, Denfield SW, Towbin JA (2010) Viral endomyocardial infection is an independent predictor and potentially treatable risk factor for graft loss and coronary vasculopathy in pediatric cardiac transplant recipients. J Am Coll Cardiol 56(7):582–592PubMed
183.
go back to reference Shaw T, Elliot P, McKenna WJ (2002) Dilated cardiomyopathy: a genetical heterogeneous disease. Lancet 360:654–655PubMed Shaw T, Elliot P, McKenna WJ (2002) Dilated cardiomyopathy: a genetical heterogeneous disease. Lancet 360:654–655PubMed
184.
go back to reference Mason JW (2003) Myocarditis and dilated cardiomyopathy: an inflammatory link. Cardiovasc Res 60:5–10PubMed Mason JW (2003) Myocarditis and dilated cardiomyopathy: an inflammatory link. Cardiovasc Res 60:5–10PubMed
185.
go back to reference Maekawa Y, Ouzounian M, Opavsky MA, Liu PP (2007) Connecting the missing link between dilated cardiomyopathy and viral myocarditis: virus, cytoskeleton, and innate immunity. Circulation 115(1):5–8PubMed Maekawa Y, Ouzounian M, Opavsky MA, Liu PP (2007) Connecting the missing link between dilated cardiomyopathy and viral myocarditis: virus, cytoskeleton, and innate immunity. Circulation 115(1):5–8PubMed
186.
go back to reference Linde A, Mosier D, Blecha F, Melgarejo T (2007) Innate immunity and inflammation–new frontiers in comparative cardiovascular pathology. Cardiovasc Res 73(1):26–36PubMed Linde A, Mosier D, Blecha F, Melgarejo T (2007) Innate immunity and inflammation–new frontiers in comparative cardiovascular pathology. Cardiovasc Res 73(1):26–36PubMed
187.
go back to reference Gorbea C, Makar KA, Pauschinger M, Pratt G, Bersola JL, Varela J, David RM, Banks L, Huang CH, Li H, Schultheiss HP, Towbin JA, Vallejo JG, Bowles NE (2010) A role for Toll-like receptor 3 variants in host susceptibility to enteroviral myocarditis and dilated cardiomyopathy. J Biol Chem 285:23208–23223PubMed Gorbea C, Makar KA, Pauschinger M, Pratt G, Bersola JL, Varela J, David RM, Banks L, Huang CH, Li H, Schultheiss HP, Towbin JA, Vallejo JG, Bowles NE (2010) A role for Toll-like receptor 3 variants in host susceptibility to enteroviral myocarditis and dilated cardiomyopathy. J Biol Chem 285:23208–23223PubMed
188.
go back to reference Mann DL (2011) The emerging role of innate immunity in the heart and vascular system: for whom the cell tolls. Circ Res 108(9):1133–1145PubMed Mann DL (2011) The emerging role of innate immunity in the heart and vascular system: for whom the cell tolls. Circ Res 108(9):1133–1145PubMed
189.
go back to reference Fuse K, Chan G, Liu Y, Gudgeon P, Husain M, Chen M, Yeh WC, Akira S, Liu PP (2005) Myeloid differentiation factor-88 plays a crucial role in the pathogenesis of coxsackievirus B3 induced myocarditis, and influences type I interferon production. Circulation 112:2276–2285PubMed Fuse K, Chan G, Liu Y, Gudgeon P, Husain M, Chen M, Yeh WC, Akira S, Liu PP (2005) Myeloid differentiation factor-88 plays a crucial role in the pathogenesis of coxsackievirus B3 induced myocarditis, and influences type I interferon production. Circulation 112:2276–2285PubMed
190.
go back to reference Mann DL, Topkara VK, Evans S, Barger PM (2010) Innate immunity in the adult mammalian heart: for whom the cell tolls. Trans Am Clin Climatol Assoc 121:34–50PubMed Mann DL, Topkara VK, Evans S, Barger PM (2010) Innate immunity in the adult mammalian heart: for whom the cell tolls. Trans Am Clin Climatol Assoc 121:34–50PubMed
191.
go back to reference Schultheiss HP, Kühl U, Cooper LT (2011) The management of myocarditis. Eur Heart J 32:2616–2625PubMed Schultheiss HP, Kühl U, Cooper LT (2011) The management of myocarditis. Eur Heart J 32:2616–2625PubMed
Metadata
Title
Viral myocarditis: from experimental models to molecular diagnosis in patients
Authors
Sabine Pankuweit
Karin Klingel
Publication date
01-11-2013
Publisher
Springer US
Published in
Heart Failure Reviews / Issue 6/2013
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI
https://doi.org/10.1007/s10741-012-9357-4

Other articles of this Issue 6/2013

Heart Failure Reviews 6/2013 Go to the issue