1887

Chapter 7 : Viral Heart Disease

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Viral Heart Disease, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819439/9781555819422.ch7-1.gif /docserver/preview/fulltext/10.1128/9781555819439/9781555819422.ch7-2.gif

Abstract:

Viral pathogens are well known to cause injury, inflammation, tissue destruction, and remodeling of heart muscle. Indeed, viruses are among the most common inciting agents to cause a condition termed acute myocarditis. This condition may also be provoked by bacteria, other pathogens, as well as toxins and autoimmune diseases, each of which could mimic the appearance of viral myocarditis. The reason for this phenotypic mimicry is that myocarditis is a process characterized pathologically by an inflammatory infiltrate of the myocardium with death or degeneration of adjacent myocytes, not typical of the ischemic damage associated with atherosclerotic coronary artery disease. The inflammation and damage may involve myocytes, interstitium, vascular elements, and pericardium. The inflammatory process affects cardiac function adversely, causing either ventricular dysfunction, arrhythmias, or both. The acute process may persist and manifest as chronic low-grade tissue inflammation and fibrosis associated with cardiomyopathy and frank heart failure.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Endomyocardial biopsy specimen from a 19-year-old man with heart failure. Histopathology includes multifocal mononuclear cell infiltrates, areas of myocardial cell death, and apparent edema. Hematoxylin and eosin (H & E) stain; scale bar, 200 μm.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

PCR analysis of fixed heart samples obtained from infants with endocardial fibroelastosis (EFE). Note the PCR-positive bands at 223 bp indicative of mumps virus. Sequence analysis confirmed the viral genome as that consistent with mumps.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Electrocardiogram from a 67-year-old man with no prior history of heart disease, normal coronary arteries, and now severe acute heart failure and viral myocarditis. Sinus tachycardia and low-voltage QRS complexes with inverted myocardial injury pattern, particularly in the inferior ventricular wall, as well as left axis deviation and right bundle branch block are present.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

hybridization for coxsackievirus B3 genome in myocardium of a newborn with lethal enteroviral myocarditis. Note replication of the virus in myocytes as visualized by radioactive RNA/RNA hybridization (black dots) in close association with mononuclear inflammatory cells. Magnification, 400×.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

(A) hybridization of acute parvovirus B19 infection of the heart is restricted to endothelial cells of small vessels as demonstrated by radioactive RNA/DNA hybridization. Cardiac inflammation is less prominent as compared to enteroviral myocarditis. Magnification, 400×. (B) PCR detection of enteroviral RNA (left panel) and parvovirus B19 DNA (right panel) by nested PCR in the myocardium of different patients with histologically proven myocarditis. Automatic DNA sequencing of viral amplification products confirms specificity of the PCR and allows the analysis of virus genotypes.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Nested PCR for the adenovirus genome. The agarose gel demonstrates a 308-bp PCR-positive band in the adenovirus-positive control lane, as well as in lanes designated MP, AD, BS, and JW, in which DNA was extracted from myocardial tissue samples obtained from patients with myocarditis. Patients designated LS and JH are PCR negative, as is the negative (–) control lane. MW, molecular weight.

Citation: McManus B, Seidman M, Klingel K, Luo H. 2017. Viral Heart Disease, p 99-113. In Richman D, Whitley R, Hayden F (ed), Clinical Virology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555819439.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819439.ch7
1. Ukimura A, Satomi H, Ooi Y, Kanzaki Y . 2012. Myocarditis associated with influenza A H1N1pdm2009. Influenza Res Treat 2012 : 351979.[PubMed]
2. Caforio AL, Pankuweit S, Arbustini E, Basso C, Gimeno-Blanes J, Felix SB, Fu M, Helio T, Heymans S, Jahns R, Klingel K, Linhart A, Maisch B, McKenna W, Mogensen J, Pinto YM, Ristic A, Schultheiss HP, Seggewiss H, Tavazzi L, Thiene G, Yilmaz A, Charron P, Elliott PM . 2013. Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 34 : 2636 2648, 2648a–2648d.
3. Cooper LT Jr . 2009. Myocarditis. N Engl J Med 360 : 1526 1538.[PubMed]
4. Kindermann I, Barth C, Mahfoud F, Ukena C, Lenski M, Yilmaz A, Klingel K, Kandolf R, Sechtem U, Cooper LT, Böhm M . 2012. Update on myocarditis. J Am Coll Cardiol 59 : 779 792.[PubMed]
5. Ni J, Bowles NE, Kim YH, Demmler G, Kearney D, Bricker JT, Towbin JA . 1997. Viral infection of the myocardium in endocardial fibroelastosis. Molecular evidence for the role of mumps virus as an etiologic agent. Circulation 95 : 133 139.[PubMed]
6. Calabrese F, Rigo E, Milanesi O, Boffa GM, Angelini A, Valente M, Thiene G . 2002. Molecular diagnosis of myocarditis and dilated cardiomyopathy in children: clinicopathologic features and prognostic implications. Diagn Mol Pathol 11 : 212 221.[PubMed]
7. Bowles NE, Towbin JA . 1998. Molecular aspects of myocarditis. Curr Opin Cardiol 13 : 179 184.[PubMed]
8. Martin AB, Webber S, Fricker FJ, Jaffe R, Demmler G, Kearney D, Zhang YH, Bodurtha J, Gelb B, Ni J . 1994. Acute myocarditis. Rapid diagnosis by PCR in children. Circulation 90 : 330 339.[PubMed]
9. Baboonian C, Davies MJ, Booth JC, McKenna WJ . 1997. Coxsackie B viruses and human heart disease. Curr Top Microbiol Immunol 223 : 31 52.[PubMed]
10. 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 : 466 472.[PubMed]
11. Hirschman SZ, Hammer GS . 1974. Coxsackie virus myopericarditis. A microbiological and clinical review. Am J Cardiol 34 : 224 232.[PubMed]
12. Woodruff JF . 1980. Viral myocarditis. A review. Am J Pathol 101 : 425 484.[PubMed]
13. Breinholt JP, Moulik M, Dreyer WJ, Denfield SW, Kim JJ, Jefferies JL, Rossano JW, Gates CM, Clunie SK, Bowles KR, Kearney DL, Bowles NE, Towbin JA . 2010. Viral epidemiologic shift in inflammatory heart disease: the increasing involvement of parvovirus B19 in the myocardium of pediatric cardiac transplant patients. J Heart Lung Transplant 29 : 739 746.[PubMed]
14. Pankuweit S, Lamparter S, Schoppet M, Maisch B . 2004. Parvovirus B19 genome in endomyocardial biopsy specimen. Circulation 109 : e179.[PubMed]
15. Francalanci P, Chance JL, Vatta M, Jimenez S, Li H, Towbin JA, Bowles NE . 2004. Cardiotropic viruses in the myocardium of children with end-stage heart disease. J Heart Lung Transplant 23 : 1046 1052.[PubMed]
16. Maisch B, Ristic AD, Portig I, Pankuweit S . 2003. Human viral cardiomyopathy. Front Biosci 8 : s39 s67.[PubMed]
17. Schowengerdt KO, Ni J, Denfield SW, Gajarski RJ, Bowles NE, Rosenthal G, Kearney DL, Price JK, Rogers BB, Schauer GM, Chinnock RE, Towbin JA . 1997. Association of parvovirus B19 genome in children with myocarditis and cardiac allograft rejection: diagnosis using the polymerase chain reaction. Circulation 96 : 3549 3554.[PubMed]
18. Wang X, Zhang G, Liu F, Han M, Xu D, Zang Y . 2004. Prevalence of human parvovirus B19 DNA in cardiac tissues of patients with congenital heart diseases indicated by nested PCR and in situ hybridization. J Clin Virol 31 : 20 24.[PubMed]
19. Matsumori A . 2005. Hepatitis C virus infection and cardiomyopathies. Circ Res 96 : 144 147.[PubMed]
20. Matsumori A . 2006. Role of hepatitis C virus in cardiomyopathies. Ernst Schering Res Found Workshop: 99 120.
21. Okabe M, Fukuda K, Arakawa K, Kikuchi M . 1997. Chronic variant of myocarditis associated with hepatitis C virus infection. Circulation 96 : 22 24.[PubMed]
22. Finland M, Parker FJ, Barnes MW, Joliffe LS . 1945. Acute myocarditis in influenza A infections: two cases of non-bacterial myocarditis, with isolation of virus from the lungs. Am J Med Sci 209 : 455 468.
23. Paddock CD, Liu L, Denison AM, Bartlett JH, Holman RC, Deleon-Carnes M, Emery SL, Drew CP, Shieh WJ, Uyeki TM, Zaki SR . 2012. Myocardial injury and bacterial pneumonia contribute to the pathogenesis of fatal influenza B virus infection. J Infect Dis 205 : 895 905.[PubMed]
24. Proby CM, Hackett D, Gupta S, Cox TM . 1986. Acute myopericarditis in influenza A infection. Q J Med 60 : 887 892.[PubMed]
25. Ukimura A, Ooi Y, Kanzaki Y, Inomata T, Izumi T . 2013. A national survey on myocarditis associated with influenza H1N1pdm2009 in the pandemic and postpandemic season in Japan. J Infect Chemother 19 : 426 431.[PubMed]
26. Schönian U, Crombach M, Maser S, Maisch B . 1995. Cytomegalovirus-associated heart muscle disease. Eur Heart J 16( Suppl O) : 46 49.[PubMed]
27. Lowry PJ, Thompson RA, Littler WA . 1983. Humoral immunity in cardiomyopathy. Br Heart J 50 : 390 394.[PubMed]
28. Ainger LE, Lawyer NG, Fitch CW . 1966. Neonatal rubella myocarditis. Br Heart J 28 : 691 697.[PubMed]
29. Lorber A, Zonis Z, Maisuls E, Dembo L, Palant A, Iancu TC . 1988. The scale of myocardial involvement in varicella myocarditis. Int J Cardiol 20 : 257 262.[PubMed]
30. Frishman W, Kraus ME, Zabkar J, Brooks V, Alonso D, Dixon LM . 1977. Infectious mononucleosis and fatal myocarditis. Chest 72 : 535 538.[PubMed]
31. Pham TV, Torres M . 2015. Human immunodeficiency virus infection-related heart disease. Emerg Med Clin North Am 33 : 613 622.[PubMed]
32. Rodriguez ER, Nasim S, Hsia J, Sandin RL, Ferreira A, Hilliard BA, Ross AM, Garrett CT . 1991. Cardiac myocytes and dendritic cells harbor human immunodeficiency virus in infected patients with and without cardiac dysfunction: detection by multiplex, nested, polymerase chain reaction in individually microdissected cells from right ventricular endomyocardial biopsy tissue. Am J Cardiol 68 : 1511 1520.[PubMed]
33. 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 1970.[PubMed]
34. 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 : 1581 1590.[PubMed]
35. Bich TD, Pham OKN, Hai DHT, Nguyen NM, Van HN, Wills B, Yacoub S . 2015. A pregnant woman with acute cardiorespiratory failure: dengue myocarditis. Lancet 385 : 1260.[PubMed]
36. Wiwanitkit S, Wiwanitkit V . 2015. Dengue myocarditis and profound shock. Am J Emerg Med 33 : 1094 1095.[PubMed]
37. Eisenhut M . 2006. Extrapulmonary manifestations of severe respiratory syncytial virus infection—a systematic review. Crit Care 10 : R107.[PubMed]
38. Weinreich MA, Jabbar AY, Malguria N, Haley RW . 2015. New-onset myocarditis in an immunocompetent adult with acute metapneumovirus infection. Case Rep Med 2015 : 814269.[PubMed]
39. Gülhan B, Kanık-Yüksek S, Çetin II, Özkaya-Parlakay A, Tezer H . 2015. Myocarditis in a child with Crimean-Congo hemorrhagic fever. Vector Borne Zoonotic Dis 15 : 565 567.[PubMed]
40. Abedi GR, Watson JT, Pham H, Nix WA, Oberste MS, Gerber SI . 2015. Enterovirus and human parechovirus surveillance—United States, 2009–2013. MMWR Morb Mortal Wkly Rep 64 : 940 943.[PubMed]
41. van der Linden L, Wolthers KC, van Kuppeveld FJM . 2015. Replication and inhibitors of enteroviruses and parechoviruses. Viruses 7 : 4529 4562.[PubMed]
42. Cristanziano VD, Böttcher S, Diedrich S, Timmen-Wego M, Knops E, Lübke N, Kaiser R, Pfister H, Kaboré Y, D'Alfonso R . 2015. Detection and characterization of enteroviruses and parechoviruses in healthy people living in the South of Côte d'Ivoire. J Clin Virol 71 : 40 43.[PubMed]
43. Lahariya C, Pradhan SK . 2006. Emergence of chikungunya virus in Indian subcontinent after 32 years: A review. J Vector Borne Dis 43 : 151 160.[PubMed]
44. Simon F, Paule P, Oliver M . 2008. Chikungunya virus-induced myopericarditis: toward an increase of dilated cardiomyopathy in countries with epidemics? Am J Trop Med Hyg 78 : 212 213.[PubMed]
45. Grist NR, Reid D, . 1988. General pathogenicity and epidemiology, p 221 239. In Bendinelli M, Friedman H (ed), Coxsackievirus: a General Update. Plenum, New York, NY.
46. Hudson REB . 1965. Myocardial involvement (myocarditis) in infections, infestation and drug therapy. Cardiovasc Pathol 1 : 782 854.
47. Wynn J, Braunwald E, . 1997. The cardiomyopathies and myocarditis, p 1404 1463. In Braunwald E (ed), Heart Disease: a Textbook of Cardiovascular Medicine. W. B. Saunders, Philadelphia, PA.
48. Mason JW . 1991. Distinct forms of myocarditis. Circulation 83 : 1110 1111.[PubMed]
49. Cooper LT Jr, Keren A, Sliwa K, Matsumori A, Mensah GA . 2014. The global burden of myocarditis: part 1: a systematic literature review for the Global Burden of Diseases, Injuries, and Risk Factors 2010 study. Glob Heart 9 : 121 129.[PubMed]
50. Van den Veyver IB, Ni J, Bowles N, Carpenter RJ Jr, Weiner CP, Yankowitz J, Moise KJ Jr, Henderson J, Towbin JA . 1998. Detection of intrauterine viral infection using the polymerase chain reaction. Mol Genet Metab 63 : 85 95.[PubMed]
51. Baboonian C, Treasure T . 1997. Meta-analysis of the association of enteroviruses with human heart disease. Heart 78 : 539 543.[PubMed]
52. Friedman RA, Schowengerdt JA, Towbin JA, . 1998. Myocarditis, p 1777 1794. In Bricker JT, Garson A Jr, Fisher DJ, Neish SR (ed), The Science and Practice of Pediatric Cardiology. Williams & Wilkins, Baltimore, MD.
53. Akhtar N, Ni J, Langston C, Demmler GJ, Towbin JA . 1996. PCR diagnosis of viral pneumonitis from fixed-lung tissue in children. Biochem Mol Med 58 : 66 76.[PubMed]
54. McManus BM, Kandolf R . 1991. Evolving concepts of cause, consequence and control in myocarditis. Curr Opin Cardiol 6 : 418 427.
55. Brownstein DG . 1998. Comparative genetics of resistance to viruses. Am J Hum Genet 62 : 211 214.[PubMed]
56. Godeny EK, Gauntt CJ . 1987. Murine natural killer cells limit coxsackievirus B3 replication. J Immunol 139 : 913 918.[PubMed]
57. Hayder H, Müllbacher A . 1996. Molecular basis of immune evasion strategies by adenoviruses. Immunol Cell Biol 74 : 504 512.[PubMed]
58. Henke A, Huber S, Stelzner A, Whitton JL . 1995. The role of CD8+ T lymphocytes in coxsackievirus B3-induced myocarditis. J Virol 69 : 6720 6728.[PubMed]
59. Hori H, Matoba T, Shingu M, Toshima H . 1981. The role of cell mediated immunity in coxsackie B viral myocarditis. Jpn Circ J 45 : 1409 1414.[PubMed]
60. Knowlton KU, Jeon ES, Berkley N, Wessely R, Huber S . 1996. A mutation in the puff region of VP2 attenuates the myocarditic phenotype of an infectious cDNA of the Woodruff variant of coxsackievirus B3. J Virol 70 : 7811 7818.[PubMed]
61. Langley RJ, Prince GA, Ginsberg HS . 1998. HIV type-1 infection of the cotton rat ( Sigmodon fulviventer and S. hispidus). Proc Natl Acad Sci USA 95 : 14355 14360.[PubMed]
62. Lee C, Maull E, Chapman N, Tracy S, Gauntt C . 1997. Genomic regions of coxsackievirus B3 associated with cardiovirulence. J Med Virol 52 : 341 347.[PubMed]
63. 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 31.[PubMed]
64. 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 1226.[PubMed]
65. 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 1453.[PubMed]
66. Huber SA . 1997. Coxsackievirus-induced myocarditis is dependent on distinct immunopathogenic responses in different strains of mice. Lab Invest 76 : 691 701.[PubMed]
67. Maisch B, Trostel-Soeder R, Stechemesser E, Berg PA, Kochsiek K . 1982. Diagnostic relevance of humoral and cell-mediated immune reactions in patients with acute viral myocarditis. Clin Exp Immunol 48 : 533 545.[PubMed]
68. Klingel K, Fabritius C, Sauter M, Göldner K, Stauch D, Kandolf R, Ettischer N, Gahlen S, Schönberger T, Ebner S, Makrigiannis AP, Bélanger S, Diefenbach A, Polić B, Pratschke J, Kotsch K . 2014. The activating receptor NKG2D of natural killer cells promotes resistance against enterovirus-mediated inflammatory cardiomyopathy. J Pathol 234 : 164 177.[PubMed]
69. Wong CY, Woodruff JJ, Woodruff JF . 1977. Generation of cytotoxic T lymphocytes during coxsackievirus tb-3 infection. II. Characterization of effector cells and demonstration cytotoxicity against viral-infected myofibers1. J Immunol 118 : 1165 1169.[PubMed]
70. 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 1582.[PubMed]
71. Marchant DJ, Bellac CL, Moraes TJ, Wadsworth SJ, Dufour A, Butler GS, Bilawchuk LM, Hendry RG, Robertson AG, Cheung CT, Ng J, Ang L, Luo Z, Heilbron K, Norris MJ, Duan W, Bucyk T, Karpov A, Devel L, Georgiadis D, Hegele RG, Luo H, Granville DJ, Dive V, McManus BM, Overall CM . 2014. A new transcriptional role for matrix metalloproteinase-12 in antiviral immunity. Nat Med 20 : 493 502.[PubMed]
72. Marchant DJ, Boyd JH, Lin DC, Granville DJ, Garmaroudi FS, McManus BM . 2012. Inflammation in myocardial diseases. Circ Res 110 : 126 144.[PubMed]
73. Marchant DJ, Cheung C, Wadsworth S, Carthy J, Ng J, Heilbron K, Luo ZS, Hegele RG, Overall CM, McManus BM . 2010. Matrixmetalloproteinase-12 regulates the antiviral immune response during viral myocarditis through interaction with gene regulatory regions. Circulation 122( 21 Suppl ) : A9085.
74. Drucker NA, Colan SD, Lewis AB, Beiser AS, Wessel DL, Takahashi M, Baker AL, Perez-Atayde AR, Newburger JW . 1994. Gamma-globulin treatment of acute myocarditis in the pediatric population. Circulation 89 : 252 257.[PubMed]
75. Bowles NE, Richardson PJ, Olsen EG, Archard LC . 1986. Detection of Coxsackie-B-virus-specific RNA sequences in myocardial biopsy samples from patients with myocarditis and dilated cardiomyopathy. Lancet 327 : 1120 1123.[PubMed]
76. Bowles NE, Rose ML, Taylor P, Banner NR, Morgan-Capner P, Cunningham L, Archard LC, Yacoub MH . 1989. End-stage dilated cardiomyopathy. Persistence of enterovirus RNA in myocardium at cardiac transplantation and lack of immune response. Circulation 80 : 1128 1136.[PubMed]
77. Dec GW Jr, Palacios IF, Fallon JT, Aretz HT, Mills J, Lee DC, Johnson RA . 1985. Active myocarditis in the spectrum of acute dilated cardiomyopathies. Clinical features, histologic correlates, and clinical outcome. N Engl J Med 312 : 885 890.[PubMed]
78. Strand S, Hofmann WJ, Hug H, Müller M, Otto G, Strand D, Mariani SM, Stremmel W, Krammer PH, Galle PR . 1996. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells—a mechanism of immune evasion? Nat Med 2 : 1361 1366.[PubMed]
79. Bowles NE, Bowles KR, Towbin JA . 2005. Viral genomic detection and outcome in myocarditis. Heart Fail Clin 1 : 407 417.[PubMed]
80. Pauschinger M, Phan MD, Doerner A, Kuehl U, Schwimmbeck PL, Poller W, Kandolf R, Schultheiss HP . 1999. Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 99 : 889 895.[PubMed]
81. Narula J, Haider N, Virmani R, DiSalvo TG, Kolodgie FD, Hajjar RJ, Schmidt U, Semigran MJ, Dec GW, Khaw BA . 1996. Apoptosis in myocytes in end-stage heart failure. N Engl J Med 335 : 1182 1189.[PubMed]
82. Hutchins GM, Vie SA . 1972. The progression of interstitial myocarditis to idiopathic endocardial fibroelastosis. Am J Pathol 66 : 483 496.[PubMed]
83. Saphir O, Field M . 1954. Complications of myocarditis in children. J Pediatr 45 : 457 463.[PubMed]
84. Chow LH, Gauntt CJ, McManus BM . 1991. Differential effects of myocarditic variants of Coxsackievirus B3 in inbred mice. A pathologic characterization of heart tissue damage. Lab Invest 64 : 55 64.[PubMed]
85. Bessoudo R, Marrie TJ, Smith ER . 1981. Cardiac involvement in trichinosis. Chest 79 : 698 699.[PubMed]
86. Brasier AR, Macklis JD, Vaughan D, Warner L, Kirshenbaum JM . 1987. Myopericarditis as an initial presentation of meningococcemia. Unusual manifestation of infection with serotype W135. Am J Med 82 : 641 644.[PubMed]
87. Leak D, Meghji M . 1979. Toxoplasmic infection in cardiac disease. Am J Cardiol 43 : 841 849.[PubMed]
88. Marsden PD . 1971. South American trypanosomiasis (Chagas’ disease). Int Rev Trop Med 4 : 97 121.[PubMed]
89. Poltera AA, Cox JN, Owor R . 1976. Pancarditis affecting the conducting system and all valves in human African trypanosomiasis. Br Heart J 38 : 827 837.[PubMed]
90. Vargo TA, Singer DB, Gillette PC, Fernbach DJ . 1977. Myocarditis due to visceral larva migrans. J Pediatr 90 : 322 323.[PubMed]
91. Burch GE, Sun SC, Sohal RS, Chu KC, Colcolough HL . 1968. Diphtheritic myocarditis. A histochemical and electron microscopic study. Am J Cardiol 21 : 261 268.[PubMed]
92. Gross D, Willens H, Zeldis SM . 1981. Myocarditis in legionnaires’ disease. Chest 79 : 232 234.[PubMed]
93. James TN . 1968. Sudden death in babies: new observations in the heart. Am J Cardiol 22 : 479 506.[PubMed]
94. Blauwet LA, Cooper LT . 2013. Idiopathic giant cell myocarditis and cardiac sarcoidosis. Heart Fail Rev 18 : 733 746.[PubMed]
95. Cooper LT Jr, . 2003. Idiopathic giant cell myocarditis. In Cooper LT Jr (ed), Myocarditis: from Bench to Bedside. Humana Press, Totowa, NJ. 405 420.
96. Davidoff R, Palacios I, Southern J, Fallon JT, Newell J, Dec GW . 1991. Giant cell versus lymphocytic myocarditis. A comparison of their clinical features and long-term outcomes. Circulation 83 : 953 961.[PubMed]
97. Maleszewski JJ, Orellana VM, Hodge DO, Kuhl U, Schultheiss HP, Cooper LT . 2015. Long-term risk of recurrence, morbidity and mortality in giant cell myocarditis. Am J Cardiol 115 : 1733 1738.[PubMed]
98. Okura Y, Dec GW, Hare JM, Kodama M, Berry GJ, Tazelaar HD, Bailey KR, Cooper LT . 2003. A clinical and histopathologic comparison of cardiac sarcoidosis and idiopathic giant cell myocarditis. J Am Coll Cardiol 41 : 322 329.[PubMed]
99. Rosenstein ED, Zucker MJ, Kramer N . 2000. Giant cell myocarditis: most fatal of autoimmune diseases. Semin Arthritis Rheum 30 : 1 16.[PubMed]
100. Stoica SC, Goddard M, Tsui S, Dunning J, McNeil K, Parameshwar J, Large SR . 2003. Ventricular assist surprise: giant cell myocarditis or sarcoidosis? J Thorac Cardiovasc Surg 126 : 2072 2074.[PubMed]
101. Shimizu C, Rambaud C, Cheron G, Rouzioux C, Lozinski GM, Rao A, Stanway G, Krous HF, Burns JC . 1995. Molecular identification of viruses in sudden infant death associated with myocarditis and pericarditis. Pediatr Infect Dis J 14 : 584 587.[PubMed]
102. Grogan M, Redfield MM, Bailey KR, Reeder GS, Gersh BJ, Edwards WD, Rodeheffer RJ . 1995. Long-term outcome of patients with biopsy-proved myocarditis: comparison with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 26 : 80 84.[PubMed]
103. Kim KS, Hufnagel G, Chapman NM, Tracy S . 2001. The group B coxsackieviruses and myocarditis. Rev Med Virol 11 : 355 368.[PubMed]
104. Friedman RA, Kearney DL, Moak JP, Fenrich AL, Perry JC . 1994. Persistence of ventricular arrhythmia after resolution of occult myocarditis in children and young adults. J Am Coll Cardiol 24 : 780 783.[PubMed]
105. English RF, Janosky JE, Ettedgui JA, Webber SA . 2004. Outcomes for children with acute myocarditis. Cardiol Young 14 : 488 493.[PubMed]
106. Mason JW, O'Connell JB, Herskowitz A, Rose NR, McManus BM, Billingham ME, Moon TE The Myocarditis Treatment Trial Investigators . 1995. A clinical trial of immunosuppressive therapy for myocarditis. N Engl J Med 333 : 269 275.[PubMed]
107. Hastreiter AR, Miller RA . 1964. Diagnosis and treatment of myocarditis and other myocardial diseases. Adv Cardiopulm Dis 22 : 250 258.[PubMed]
108. Towbin JA, Bricker JT, Garson A Jr . 1992. Electrocardiographic criteria for diagnosis of acute myocardial infarction in childhood. Am J Cardiol 69 : 1545 1548.[PubMed]
109. Mantke OD, Meyer R, Prösch S, Nitsche A, Leitmeyer K, Kallies R, Niedrig M . 2005. High prevalence of cardiotropic viruses in myocardial tissue from explanted hearts of heart transplant recipients and heart donors: a 3-year retrospective study from a German patients’ pool. J Heart Lung Transplant 24 : 1632 1638.[PubMed]
110. Matsumori A . 1997. Molecular and immune mechanisms in the pathogenesis of cardiomyopathy—role of viruses, cytokines, and nitric oxide. Jpn Circ J 61 : 275 291.[PubMed]
111. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J . 2005. Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol 45 : 1815 1822.[PubMed]
112. Baccouche H, Mahrholdt H, Meinhardt G, Merher R, Voehringer M, Hill S, Klingel K, Kandolf R, Sechtem U, Yilmaz A . 2009. Diagnostic synergy of non-invasive cardiovascular magnetic resonance and invasive endomyocardial biopsy in troponin-positive patients without coronary artery disease. Eur Heart J 30 : 2869 2879.[PubMed]
113. Friedrich MG, Marcotte F . 2013. Cardiac magnetic resonance assessment of myocarditis. Circ Cardiovasc Imaging 6 : 833 839.[PubMed]
114. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, White JA, Abdel-Aty H, Gutberlet M, Prasad S, Aletras A, Laissy JP, Paterson I, Filipchuk NG, Kumar A, Pauschinger M, Liu P International Consensus Group on Cardiovascular Magnetic Resonance in M . 2009. Cardiovascular magnetic resonance in myocarditis: a JACC white paper. J Am Coll Cardiol 53 : 1475 1487.
115. Mahrholdt H, Goedecke C, Wagner A, Meinhardt G, Athanasiadis A, Vogelsberg H, Fritz P, Klingel K, Kandolf R, Sechtem U . 2004. Cardiovascular magnetic resonance assessment of human myocarditis: a comparison to histology and molecular pathology. Circulation 109 : 1250 1258.[PubMed]
116. Canter CE, Simpson KP . 2014. Diagnosis and treatment of myocarditis in children in the current era. Circulation 129 : 115 128.[PubMed]
117. Kemp M, Donovan J, Higham H, Hooper J . 2004. Biochemical markers of myocardial injury. Br J Anaesth 93 : 63 73.[PubMed]
118. Smith SC, Ladenson JH, Mason JW, Jaffe AS . 1997. Elevations of cardiac troponin I associated with myocarditis. Experimental and clinical correlates. Circulation 95 : 163 168.[PubMed]
119. Aretz HT . 1987. Myocarditis: the Dallas criteria. Hum Pathol 18 : 619 624.[PubMed]
120. Chow LH, Radio SJ, Sears TD, McManus BM . 1989. Insensitivity of right ventricular endomyocardial biopsy in the diagnosis of myocarditis. J Am Coll Cardiol 14 : 915 920.[PubMed]
121. Hauck AJ, Kearney DL, Edwards WD . 1989. Evaluation of postmortem endomyocardial biopsy specimens from 38 patients with lymphocytic myocarditis: implications for role of sampling error. Mayo Clin Proc 64 : 1235 1245.[PubMed]
122. Shingu M . 1989. Laboratory diagnosis of viral myocarditis. A review. Jpn Circ J 53 : 87 93.[PubMed]
123. Martino TA, Liu P, Sole MJ . 1994. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ Res 74 : 182 188.[PubMed]
124. Baughman KL . 2006. Diagnosis of myocarditis: death of Dallas criteria. Circulation 113 : 593 595.[PubMed]
125. Abbate A, Sinagra G, Bussani R, Hoke NN, Merlo M, Varma A, Toldo S, Salloum FN, Biondi-Zoccai GG, Vetrovec GW, Crea F, Silvestri F, Baldi A . 2009. Apoptosis in patients with acute myocarditis. Am J Cardiol 104 : 995 1000.[PubMed]
126. Saraste A, Arola A, Vuorinen T, Kytö V, Kallajoki M, Pulkki K, Voipio-Pulkki LM, Hyypiä T . 2003. Cardiomyocyte apoptosis in experimental coxsackievirus B3 myocarditis. Cardiovasc Pathol 12 : 255 262.[PubMed]
127. Zorc-Pleskovic R, Alibegović A, Zorc M, Milutinović A, Radovanović N, Petrović D . 2006. Apoptosis of cardiomyocytes in myocarditis. Folia Biol (Praha) 52 : 6 9.[PubMed]
128. Piedra PA, Poveda GA, Ramsey B, McCoy K, Hiatt PW . 1998. Incidence and prevalence of neutralizing antibodies to the common adenoviruses in children with cystic fibrosis: implication for gene therapy with adenovirus vectors. Pediatrics 101 : 1013 1019.[PubMed]
129. Sole MJ, Liu P . 1993. Viral myocarditis: a paradigm for understanding the pathogenesis and treatment of dilated cardiomyopathy. J Am Coll Cardiol 22( Suppl A) : A99 A105.[PubMed]
130. Kandolf R, . 1988. The impact of recombinant DNA technology on the study of enteroviral heart disease, p 293 318. In Bendinelli M, Friedman H (ed), Coxsackievirus: a General Undate. Plenum, New York, NY.
131. Hohenadl C, Klingel K, Mertsching J, Hofschneider PH, Kandolf R . 1991. Strand-specific detection of enteroviral RNA in myocardial tissue by in situ hybridization. Mol Cell Probes 5 : 11 20.[PubMed]
132. 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 : 314 318.[PubMed]
133. Archard LC, Khan MA, Soteriou BA, Zhang H, Why HJ, Robinson NM, Richardson PJ . 1998. Characterization 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.[PubMed]
134. Pauschinger M, Bowles NE, Fuentes-Garcia FJ, Pham V, Kühl U, Schwimmbeck PL, Schultheiss HP, Towbin JA . 1999. Detection of adenoviral genome in the myocardium of adult patients with idiopathic left ventricular dysfunction. Circulation 99 : 1348 1354.[PubMed]
135. Weiss LM, Liu XF, Chang KL, Billingham ME . 1992. Detection of enteroviral RNA in idiopathic dilated cardiomyopathy and other human cardiac tissues. J Clin Invest 90 : 156 159.[PubMed]
136. Daliento L, Calabrese F, Tona F, Caforio AL, Tarsia G, Angelini A, Thiene G . 2003. Successful treatment of enterovirus-induced myocarditis with interferon-alpha. J Heart Lung Transplant 22 : 214 217.[PubMed]
137. Jin O, Sole MJ, Butany JW, Chia WK, McLaughlin PR, Liu P, Liew CC . 1990. Detection of enterovirus RNA in myocardial biopsies from patients with myocarditis and cardiomyopathy using gene amplification by polymerase chain reaction. Circulation 82 : 8 16.[PubMed]
138. Hidron A, Vogenthaler N, Santos-Preciado JI, Rodriguez-Morales AJ, Franco-Paredes C, Rassi A Jr . 2010. Cardiac involvement with parasitic infections. Clin Microbiol Rev 23 : 324 349.[PubMed]
139. Karjalainen J . 1989. Streptococcal tonsillitis and acute nonrheumatic myopericarditis. Chest 95 : 359 363.[PubMed]
140. Lewes D, Rainford DJ, Lane WF . 1974. Symptomless myocarditis and myalgia in viral and Mycoplasma pneumoniae infections. Br Heart J 36 : 924 932.[PubMed]
141. Marin-Garcia J, Barrett FF . 1983. Myocardial function in Rocky Mountain spotted fever: echocardiographic assessment. Am J Cardiol 51 : 341 343.[PubMed]
142. McAlister HF, Klementowicz PT, Andrews C, Fisher JD, Feld M, Furman S . 1989. Lyme carditis: an important cause of reversible heart block. Ann Intern Med 110 : 339 345.[PubMed]
143. Grenade LL, Graham D, Trontell A . 2001. Myocarditis and cardiomyopathy associated with clozapine use in the United States. N Engl J Med 345 : 224 225.[PubMed]
144. Gaudin PB, Hruban RH, Beschorner WE, Kasper EK, Olson JL, Baughman KL, Hutchins GM . 1993. Myocarditis associated with doxorubicin cardiotoxicity. Am J Clin Pathol 100 : 158 163.[PubMed]
145. Fairley SL, Herron B, Wilson CM, Roberts MJ . 2014. Acute fulminant necrotising lymphocytic myocarditis in a patient with mixed connective tissue disease: a rapid clinical response to immunosuppression. Ulster Med J 83 : 119 120.[PubMed]
146. Ferrans VJ, Rodríguez ER . 1985. Cardiovascular lesions in collagen-vascular diseases. Heart Vessels Suppl 1( S1) : 256 261.[PubMed]
147. Kerr LD, Spiera H . 1993. Myocarditis as a complication in scleroderma patients with myositis. Clin Cardiol 16 : 895 899.[PubMed]
148. Lash AD, Wittman AL, Quismorio FP Jr . 1986. Myocarditis in mixed connective tissue disease: clinical and pathologic study of three cases and review of the literature. Semin Arthritis Rheum 15 : 288 296.[PubMed]
149. Miner JJ, Kim AH . 2014. Cardiac manifestations of systemic lupus erythematosus. Rheum Dis Clin North Am 40 : 51 60.[PubMed]
150. Spina GS, Sampaio RO, Branco CE, Miranda GB, Rosa VE, Tarasoutchi F . 2014. Incidental histological diagnosis of acute rheumatic myocarditis: case report and review of the literature. Front Pediatr 2 : 126.[PubMed]
151. Xavier JL Jr, Matos Soeiro A, Lopes AS, Spina GS, Serrano CV Jr, Oliveira MT Jr . 2014. Clinically manifested myocarditis in acute rheumatic fever. Arq Bras Cardiol 102 : e17 e20.[PubMed]
152. Chaudary S, Jaski BE . 1989. Fulminant mumps myocarditis. Ann Intern Med 110 : 569 570.[PubMed]
153. Nunes H, Freynet O, Naggara N, Soussan M, Weinman P, Diebold B, Brillet PY, Valeyre D . 2010. Cardiac sarcoidosis. Semin Respir Crit Care Med 31 : 428 441.[PubMed]
154. Yamamoto LG . 2003. Kawasaki disease. Pediatr Emerg Care 19 : 422 424.[PubMed]
155. Pollack A, Kontorovich AR, Fuster V, Dec GW . 2015. Viral myocarditis—diagnosis, treatment options, and current controversies. Nat Rev Cardiol 12 : 670 680.[PubMed]
156. Bengtsson E, Lamberger B . 1966. Five-year follow-up study of cases suggestive of acute myocarditis. Am Heart J 72 : 751 763.
157. Felker GM, Jaeger CJ, Klodas E, Thiemann DR, Hare JM, Hruban RH, Kasper EK, Baughman KL . 2000. Myocarditis and long-term survival in peripartum cardiomyopathy. Am Heart J 140 : 785 791.[PubMed]
158. McCarthy RE III, Boehmer JP, Hruban RH, Hutchins GM, Kasper EK, Hare JM, Baughman KL . 2000. Long-term outcome of fulminant myocarditis as compared with acute (nonfulminant) myocarditis. N Engl J Med 342 : 690 695.[PubMed]
159. Towbin JA . 1998. The role of cytoskeletal proteins in cardiomyopathies. Curr Opin Cell Biol 10 : 131 139.[PubMed]
160. Badorff C, Lee GH, Lamphear BJ, Martone ME, Campbell KP, Rhoads RE, Knowlton KU . 1999. Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat Med 5 : 320 326.[PubMed]
161. Lim BK, Peter AK, Xiong D, Narezkina A, Yung A, Dalton ND, Hwang KK, Yajima T, Chen J, Knowlton KU . 2013. Inhibition of Coxsackievirus-associated dystrophin cleavage prevents cardiomyopathy. J Clin Invest 123 : 5146 5151.[PubMed]
162. Xiong D, Yajima T, Lim BK, Stenbit A, Dublin A, Dalton ND, Summers-Torres D, Molkentin JD, Duplain H, Wessely R, Chen J, Knowlton KU . 2007. Inducible cardiac-restricted expression of enteroviral protease 2A is sufficient to induce dilated cardiomyopathy. Circulation 115 : 94 102.[PubMed]
163. Towbin JA . 2002. Cardiomyopathy and heart transplantation in children. Curr Opin Cardiol 17 : 274 279.[PubMed]
164. Towbin JA, Bowles NE . 2002. The failing heart. Nature 415 : 227 233.[PubMed]
165. Calabrese F, Thiene G . 2003. Myocarditis and inflammatory cardiomyopathy: microbiological and molecular biological aspects. Cardiovasc Res 60 : 11 25.[PubMed]
166. Grumbach IM, Heim A, Pring-Akerblom P, Vonhof S, Hein WJ, Müller G, Figulla HR . 1999. Adenoviruses and enteroviruses as pathogens in myocarditis and dilated cardiomyopathy. Acta Cardiol 54 : 83 88.[PubMed]
167. O'Connell JB , et al . 1990. Results of heart transplantation for active lymphocytic myocarditis. J Heart Transplant 9 : 351 355, discussion 355–356.[PubMed]
168. O'Connell JB, Fowles RE, Robinson JA, Subramanian R, Henkin RE, Gunnar RM . 1984. Clinical and pathologic findings of myocarditis in two families with dilated cardiomyopathy. Am Heart J 107 : 127 135.[PubMed]
169. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW . 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275 : 1320 1323.[PubMed]
170. 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 3356.[PubMed]
171. Chen JW, Zhou B, Yu QC, Shin SJ, Jiao K, Schneider MD, Baldwin HS, Bergelson JM . 2006. Cardiomyocyte-specific deletion of the coxsackievirus and adenovirus receptor results in hyperplasia of the embryonic left ventricle and abnormalities of sinuatrial valves. Circ Res 98 : 923 930.[PubMed]
172. Lim BK, Xiong D, Dorner A, Youn TJ, Yung A, Liu TI, Gu Y, Dalton ND, Wright AT, Evans SM, Chen J, Peterson KL, McCulloch AD, Yajima T, Knowlton KU . 2008. Coxsackievirus and adenovirus receptor (CAR) mediates atrioventricular-node function and connexin 45 localization in the murine heart. J Clin Invest 118 : 2758 2770.[PubMed]
173. Lisewski U, Shi Y, Wrackmeyer U, Fischer R, Chen C, Schirdewan A, Jüttner R, Rathjen F, Poller W, Radke MH, Gotthardt M . 2008. The tight junction protein CAR regulates cardiac conduction and cell-cell communication. J Exp Med 205 : 2369 2379.[PubMed]
174. Bergelson JM, Mohanty JG, Crowell RL, St John