• Users Online: 409
  • Print this page
  • Email this page

Table of Contents
Year : 2020  |  Volume : 9  |  Issue : 1  |  Page : 1-13

Global study of viral myocarditis: A systematic review and meta-analysis

1 Department of Microbiology, School of Medicine; Non Communicable Diseases Research Center, Alborz University of Medical Sciences, Karaj, Iran
2 Department of Pathobiology, School of Public Health; Students Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran
3 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Submission07-Dec-2019
Date of Decision27-Dec-2019
Date of Acceptance08-Jan-2020
Date of Web Publication24-Jan-2020

Correspondence Address:
Ebrahim Faghihloo
Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran
Login to access the Email id

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2221-6189.276076

Rights and Permissions

Objective: To investigate the prevalence of viral myocarditis worldwide.
Methods: We conducted a systematic search for the prevalence of the most common viruses in myocarditis and 75 studies were included for statistical analysis of the prevalence of adenovirus, hepatitis C virus, cytomegalovirus, Ebola virus, human herpesvirus 6, influenza virus, parvovirus, and non-polio enteroviruses.
Results: The highest prevalence was related to B19 (25.0%) and non-polio enteroviruses (18%). The prevalence of human herpesvirus 6, cytomegalovirus, and Ebola virus was12.8%, 5.5%, and 3.1%, respectively. Hepatitis C virus accounted for 6.1% of the disease, the adenoviruses contributed to 5.2% of viral myocarditis. The lowest incidence was related to the influenza virus with 2.0%.
Conclusions: Treatment of myocarditis is still problematic and may depend on the etiologic diagnosis. So it is important to know the commonly occurring viral factors in myocarditis and timely diagnosis and treatment are also imperative.

Keywords: Virus; Myocarditis; Meta-analysis; B19; Non-polio enteroviruses

How to cite this article:
Dadashi M, Azimi T, Faghihloo E. Global study of viral myocarditis: A systematic review and meta-analysis. J Acute Dis 2020;9:1-13

How to cite this URL:
Dadashi M, Azimi T, Faghihloo E. Global study of viral myocarditis: A systematic review and meta-analysis. J Acute Dis [serial online] 2020 [cited 2022 Oct 5];9:1-13. Available from: https://www.jadweb.org/text.asp?2020/9/1/1/276076

Masoud Dadashi, Taher Azimi. Both of the authors contributed equally to this work.

  1. Introduction Top

Myocarditis is a multi-factorial disease of the myocardium with a large number of risk factors that are particularly attributed to multiple infectious and non-infectious agents[1],[2]. Globally, the occurrence of myocarditis is around 1.5 million cases annually, and the incidence of myocarditis was 10 to 20 per 100 000 worldwide[3]. Moreover, it is the main reason for the severe heart failure among all age groups, especially children and adults aged <40 years[4]. The clinical symptoms of myocarditis are variable, including asymptomatic courses, chest pain, congestive heart failure, syncope, cardiogenic shock, cardiac arrest and even sudden death, and other severe illness with the necessity of intensive care therapy[2],[5],[6]. According to the immunohistological evaluation of endomyocardial biopsies, clinicopathological and clinical criteria, the diagnosis and classification of myocarditis have been conducted[7-9]. Several autoimmune disorders such as Wegener’s granulomatosis, systemic lupus erythematosus, and giant cell arteritis belong to non- infectious causes of myocarditis[5],[10]. However, among infectious causes, viral infections are the main reasons for inflammatory dilated cardiomyopathy and myocarditis. In the different parts of the world, especially in Europe and North America, myocarditis is caused predominantly by viral infections[1],[4],[11]. Moreover, it is predicted that 35% to 50% of dilated cardiomyopathy has been caused by viral myocarditis (VMC)[1],[2],[11]. The finding of several studies indicated that molecular pathological analyses, such as polymerase chain reaction and in situ hybridization, as well as serological analyses, could be applied for fast and comprehensive identification of viral myocardial infection[1],[6],[12],[13]. Generally, the occurrence and prevalence of VMC is principally based on 3 types of evidence: (1) Detection rate of VMC at immunohistological evaluation of endomyocardial biopsies as the gold standard method; (2) High prevalence of myocarditis disease during the period of virus infection outbreaks; (3) Percentage of VMC out of all infection diseases in a definite province and a particular population[2]. Viral infections include adenovirus, enteroviruses, particularly coxsackievirus B, as well as parvovirus (B19) and human herpesvirus 6 (HHV-6) are related to VMC[4],[11]. Previously published studies revealed that viral nucleic acids in the myocardium in patients with myocarditis were high[14],[15], while information from distinct studies regarding the interaction between different viral family and myocarditis is not entirely consistent. For this purpose, we focused on the relationship of viral infection and myocarditis and we conducted a systematic review and meta-analysis with no language restriction.

  2. Materials and methods Top

2.1. Literature search

We conducted a systematic search for the prevalence of the most common viruses in myocarditis including adenovirus, hepatitis C virus (HCV), herpesviruses including cytomegalovirus (CMV), Ebola virus (EBV), and human herpes virus (HHV) 6, influenza virus, B19 and non-polio enteroviruses based on scientific keywords “Myocarditis” or “Heart disease” and “Viral infection” or “Viral myocarditis” and their synonyms by using three main electronic databases of Medline (via PubMed), Embase, and Web of Science from October 1973 to September 2017. The search was limited to the original articles published in English that indicated the prevalence or incidence of mentioned viruses in different parts of the world. We also searched the bibliographies for any retrieved articles for additional references.

2.2. Inclusion and exclusion criteria

All of the original papers presenting cross-sectional studies on the prevalence of the most common viruses were evaluated perspicuously. The selected studies were analyzed based on titles, abstracts, and full texts. The entire recorded studies included in our analysis based on the following criteria: (1) Original articles that provided sufficient data; (2) With standard methods, including serology methods, immunohistochemistry assay, and molecular methods to detect adenovirus, HCV, CMV, EBC, HHV6, Influenza virus, B19, and non-polio enteroviruses. The exclusion criteria were: (1) Articles studying non-human samples; (2) Case reports; (3) reviews (4) Abstracts reported in conferences; (5) Duplicate articles for the same investigation.

2.3. Data extraction and definitions

The author’s first name, the date for the investigation, year of publication, country/continent, number of the most common viruses in myocarditis, detection method and the source of isolates were extracted from included studies. Deliberately, the information on the prevalence of adenovirus, HCV, CMV, EBC, HHV6, influenza virus, B19, and non-polio enteroviruses was extracted; concurrently, two people recorded the data from all articles independently without any bias.

2.4. Quality assessment

All reviewed studies were assessed based on the quality assessment checklist (designed by the Joanna Briggs Institute), and only high- quality investigations were evaluated in the final analysis in this study based on mentioned including criteria.

2.5. Meta-analysis

The analysis was performed using STATA (version 14.0) software. The data were pooled using the fixed-effects model[16] and the random-effects model[17]. Statistical heterogeneity was assessed using Cochran Q and I2 statistical methods[18].

  3. Results Top

3.1. Characteristics of included studies

In total, we identified a total of 2 152 articles in the mentioned databases search. Based on the title and abstract evaluation, after the secondary screening, 1 992 articles were excluded. Upon a fulltext review, 84 out of 160 studies were excluded. Ultimately 75 studies were included for statistical analysis of the prevalence of adenovirus, HCV, CMV, EBC, HHV6, influenza virus, B19, and non-polio enteroviruses respectively, based on the inclusion and exclusion criteria [Supplementary Figure 1] [Additional file 1]. These 75 articles that indicated the prevalence of the most common viruses is shown in [Table 1]. The majority of studies were from Germany (n=22), USA (n=14), Italy (n=10), Japan (n= 6), and England (n=5), respectively[19-83].
Table 1: Studies used in the meta-analysis.

Click here to view

3.2. The prevalence of adenovirus, HCV, CMV, EBC, HHV6, influenza virus, B19, and non-polio enteroviruses

Eloquently, the pooled prevalence of adenovirus, HCV, CMV, EBV, HHV6, influenza virus, B19 and non-polio enteroviruses were 5.2% (95% CI: 3.3-7.0) among 1 355 patients, 6.1% (95% CI: 1.8-10.4) among 413 patients, 5.5% (95% CI: 3.3-7.7) among 1 648 patients, and 3.1% (95% CI: 1.7-4.6) among 1 952 patients, 12.8% (95% CI: 8.8-16.7) among 3 003 isolate, 2.0% (95% CI: 0.5-3.4) among 891 patients, 25.0% (95% CI: 20.0-29.0) among 3 840 patients and 18 % (95% CI: 4.7-11.1) among 599 patients respectively [Figure 1],[Figure 2],[Figure 3],[Figure 4],[Figure 5],[Figure 6],[Figure 7],[Figure 8].
Figure 1: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of B19 in patients with myocarditis.

Click here to view
Figure 2: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of human herpes virus 6 in patients with myocarditis.

Click here to view
Figure 3: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of influenza in patients with myocarditis.

Click here to view
Figure 4: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of hepatitis C virus in patients with myocarditis.

Click here to view
Figure 5: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of non-polio enteroviruses in patients with myocarditis.

Click here to view
Figure 6: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of cytomegalovirus in patients with myocarditis.

Click here to view
Figure 7: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of Ebola virus in patients with myocarditis.

Click here to view
Figure 8: Forest plot (A), funnel plot (B) and Galbraith (C) of the meta-analysis on prevalence of adeno in patients with myocarditis.

Click here to view

  4. Discussion Top

VMC includes inflammatory cardiomyopathy caused by viruses, which is one of the common diseases of heart disease. The disease is on the rise and is now becoming a common cardiovascular disease after coronary heart disease. It can occur in all age groups, from infants to the elderly, but mainly in children and adults under the age of 40[84].

The clinical course of VMC manifests itself with various cardiac symptoms including breathing difficulty, fatigue, exercise intolerance, chest pain, severe heart failure and arrhythmia and maybe non-symptom[85]. It sometimes mimics myocardial infarction. Sixty percent of patients presented arthralgia, fever, sweating, respiratory or gastrointestinal symptoms 1-2 weeks before disease[86].

Since the 1970s, the incidence of VMC has been continuing to grow in China, Japan, and other countries, and a large amount of clinical information has been reported. However, its pathogenesis is still unclear. Considering the rapid development of molecular biology in recent years, great progress has been made in this field. Almost, all human virus infections can involve the heart. It has been found that more than 30 kinds of viruses can cause myocarditis.

Since the incidence of myocarditis is high in the 21st century, understanding the epidemiological characteristics of the viral causes of the disease is important[84].

The prevalence of adenovirus, HCV, CMV, EBV, HHV6, influenza virus, B19, and non-polio enteroviruses are calculated using 75 studies based on the inclusion and exclusion criteria. This meta-analysis shows that the highest prevalence is related to B19 and non-polio enteroviruses prevalence were 25.0% (95% CI: 20.029.0) and 18% (95% CI: 4.7-11.1) respectively. The prevalence of viruses belonging to the herpes virus family includes HHV6, CMV, EBV (12.8%, 95% CI: 8.8-16.7; 5.5%, 95% CI: 3.3-7.7; and 3.1%, 95% CI: 1.7-4.6, respectively).

HCV accounted for 6.1% (95% CI: 1.8-10.4) of the disease, while the adenoviruses leded to 5.2% (95% CI: 3.3-7.0) VMC. The lowest incidence was related to influenza virus with 2.0% (95% CI: 0.5-3.4).

Several studies have found that some viruses are the main cause of myocarditis. For example, most researchers believe that enteroviruses are the most common cause of VMC. Whereas Kühl et al. reported that the parvovirus B19 genome could be in about 51.4% of VMC cases[87]. However, Griffin et al. found that VMC patients were mostly infected with adenovirus[88].

The result of this meta-analysis shows that B19 is the most common cause of VMC and non-polio enteroviruses are the second.

In conclusion, whereas effective commercial medications are available for some viruses that cause myocarditis such as ganciclovir for CMV and oseltamivir for influenza, a rapid and correct diagnosis could lead to the prevention of further disorders and the treatment of this infections.

There were some limitations in this study that should be discussed. First, as with any systematic review and meta-analysis, the existence of publication bias must be taken into account. Second, heterogeneity was observed among the evaluated articles. Although the random-effects model allows for heterogeneity, there may still be differences of opinion regarding the composition of the studies.

Conflict of interest statement

The authors report no conflict of interest.

Authors’ contribution

M.D. and E.F. conceived and designed the study. T.A. and M.D. contributed in comprehensive research. M.D. and T.A. analyzed the data. M.D., T.A., and E.F. wrote the paper. M.D. and F.F. participated in data analysis and manuscript editing.

  References Top

Mahfoud F, Gärtner B, Kindermann M, Ukena C, Gadomski K, Klingel K, et al. Virus serology in patients with suspected myocarditis: utility or futility? Eur Heart J 2011; 32(7): 897-903.  Back to cited text no. 1
Lv S, Rong J, Ren S, Wu M, Li M, Zhu Y, et al. Epidemiology and diagnosis of viral myocarditis. Hellenic J Cardiol 2013; 54(5): 382-391.  Back to cited text no. 2
Pollack A, Kontorovich AR, Fuster V, Dec GW. Viral myocarditis-diagnosis, treatment options, and current controversies. Nat Rev Cardiol 2015; 12(11): 670-680.  Back to cited text no. 3
Mahrholdt H, Wagner A, Deluigi CC, Kispert E, Hager S, Meinhardt G, et al. Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation 2006; 114(15): 1581-1590.  Back to cited text no. 4
Calabrese F, Carturan E, Chimenti C, Pieroni M, Agostini C, Angelini A, et al. Overexpression of tumor necrosis factor (TNF) α and TNF receptor I in human viral myocarditis: clinicopathologic correlations. Mod Pathol 2004; 17(9): 1108.  Back to cited text no. 5
Calabrese F, Rigo E, Milanesi O, Boffa GM, Angelini A, Valente M, et al. Molecular diagnosis of myocarditis and dilated cardiomyopathy in children: clinicopathologic features and prognostic implications. Diagn Mol Pathol 2002; 11(4): 212-221.  Back to cited text no. 6
Caforio AL, Calabrese F, Angelini A, Tona F, Vinci A, Bottaro S, et al. A prospective study of biopsy-proven myocarditis: prognostic relevance of clinical and aetiopathogenetic features at diagnosis. Eur Heart J 2007; 28(11): 1326-1333.  Back to cited text no. 7
Pauschinger M, Noutsias M, Lassner D, Schultheiss H-P, Kuehl U. Inflammation, ECG changes and pericardial effusion. Clin Res Cardiol 2006; 95(11): 569-583.  Back to cited text no. 8
Mahrholdt H, Goedecke C, Wagner A, Meinhardt G, Athanasiadis A, Vogelsberg H, et al. Cardiovascular magnetic resonance assessment of human myocarditis: a comparison to histology and molecular pathology. Circulation 2004; 109(10): 1250-1258.  Back to cited text no. 9
O’Connell JB. The role of myocarditis in end-stage dilated cardiomyopathy. Tex Heart Inst J 1987; 14(3): 268-275.  Back to cited text no. 10
Pawlak A, Przybylski M, Durlik M, Gil K, Nasierowska-Guttmejer AM, Byczkowska K, et al. Viral nucleic acids in the serum are dependent on blood sampling site in patients with clinical suspicion of myocarditis. Intervirology 2016; 59(3): 143-151.  Back to cited text no. 11
Angelini A, Crosato M, Boffa G, Calabrese F, Calzolari V, Chioin R, et al. Active versus borderline myocarditis: clinicopathological correlates and prognostic implications. Heart 2002; 87(3): 210-215.  Back to cited text no. 12
Richardson P, McKenna W, Bristow M, Maisch B, Mautner BO, Connell J, et al. Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies. Circulation 1996; 93: 841-842.  Back to cited text no. 13
Comar M, D’agaro P, Campello C, Poli A, Breinholt J, Towbin J, et al. Human herpes virus 6 in archival cardiac tissues from children with idiopathic dilated cardiomyopathy or congenital heart disease. J Clin Pathol 2009; 62(1): 80-83.  Back to cited text no. 14
Chimenti C, Russo A, Pieroni M, Calabrese F, Verardo R, Thiene G, et al. Intramyocyte detection of Epstein-Barr virus genome by laser capture microdissection in patients with inflammatory cardiomyopathy. Circulation 2004; 110(23): 3534-3539.  Back to cited text no. 15
Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959; 22(4): 719-748.  Back to cited text no. 16
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7(3): 177-188.  Back to cited text no. 17
Higgins J, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Medicine 2002; 21(11): 1539-1558.  Back to cited text no. 18
Bowles NE, Ni J, Kearney DL, Pauschinger M, Schultheiss HP, McCarthy R, et al. 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 2003; 42(3): 466-472.  Back to cited text no. 19
Fujioka S, Kitaura Y, Ukimura A, Deguchi H, Kawamura K, Isomura T, et al. Evaluation of viral infection in the myocardium of patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2000; 36(6): 19201926.  Back to cited text no. 20
Grün S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, et al. Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery. J Am Coll Cardiol 2012; 59(18): 1604-1615.  Back to cited text no. 21
Nielsen TS, Nielsen AY, Banner J, Hansen J, Baandrup U, Nielsen LP. Saffold virus infection associated with human myocarditis. J Clin Virol 2016; 74: 78-81.  Back to cited text no. 22
Boudjellil R, Elbaz M, Lairez O, Lhomme S, Izopet J, Kamar N. No evidence of genotype-3 hepatitis E virus-induced myocarditis. J Clin Virol 2016; 76: 44.  Back to cited text no. 23
Kühl U, Lassner D, Wallaschek N, Gross UM, Krueger GR, Seeberg B, et al. Chromosomally integrated human herpesvirus 6 in heart failure: prevalence and treatment. Eur J Heart Fail 2015; 17(1): 9-19.  Back to cited text no. 24
Ukimura A, Izumi T, Matsumori A. A national survey on myocarditis associated with the 2009 influenza A (H1N1) pandemic in Japan. Circ J 2010; 74(10): 2193-2199.  Back to cited text no. 25
Li Y, Bourlet T, Andreoletti L, Mosnier J-F, Peng T, Yang Y, et al. Enteroviral capsid protein VP1 is present in myocardial tissues from some patients with myocarditis or dilated cardiomyopathy. Circulation 2000; 101(3): 231-234.  Back to cited text no. 26
Kühl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, et al. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with “idiopathic” left ventricular dysfunction. Circulation 2005; 111(7): 887-893.  Back to cited text no. 27
Schowengerdt KO, Ni J, Denfield SW, Gajarski RJ, Bowles NE, Rosenthal G, et al. Association of parvovirus B19 genome in children with myocarditis and cardiac allograft rejection: diagnosis using the polymerase chain reaction. Circulation 1997; 96(10): 3549-3554.  Back to cited text no. 28
Gaaloul I, Riabi S, Harrath R, Hunter T, Hamda KB, Ghzala AB, et al. Coxsackievirus B detection in cases of myocarditis, myopericarditis, pericarditis and dilated cardiomyopathy in hospitalized patients. Mol Med Rep 2014; 10(6): 2811-2818.  Back to cited text no. 29
Simpson KE, Storch GA, Lee CK, Ward KE, Danon S, Simon CM, et al. High frequency of detection by PCR of viral nucleic acid in the blood of infants presenting with clinical myocarditis. Pediatr Cardiol 2016; 37(2): 399-404.  Back to cited text no. 30
Pauschinger M, Bowles NE, Fuentes-Garcia FJ, Pham V, Kühl U, Schwimmbeck PL, et al. Detection of adenoviral genome in the myocardium of adult patients with idiopathic left ventricular dysfunction. Circulation 1999; 99(10): 1348-1354.  Back to cited text no. 31
Schmidt NJ, Magoffin RL, Lennette EH. Association of group B coxsackieviruses with cases of pericarditis, myocarditis, or pleurodynia by demonstration of immunoglobulin M antibody. Infect Immun 1973; 8(3): 341-348.  Back to cited text no. 32
Gagliardi MG, Fierabracci A, Pilati M, Chinali M, Bassano C, Saura F, et al. The impact of specific viruses on clinical outcome in children presenting with acute heart failure. Int J Mol Sci 2016; 17(4): 486.  Back to cited text no. 33
Nicholson F, Ajetunmobi J, Li M, Shackleton E, Starkey W, Illavia S, et al. Molecular detection and serotypic analysis of enterovirus RNA in archival specimens from patients with acute myocarditis. Heart 1995; 74(5): 522-527.  Back to cited text no. 34
Griffin LD, Kearney D, Ni J, Jaffe R, Fricker FJ, Webber S, et al. Analysis of formalin-fixed and frozen myocardial autopsy samples for viral genome in childhood myocarditis and dilated cardiomyopathy with endocardial fibroelastosis using polymerase chain reaction (PCR). Cardiovasc Pathol 1995; 4(1): 3-11.  Back to cited text no. 35
Andréoletti L, Ventéo L, Douche-Aourik F, Canas F, de la Grandmaison GL, Jacques J, et al. Active Coxsackieviral B infection is associated with disruption of dystrophin in endomyocardial tissue of patients who died suddenly of acute myocardial infarction. J Am Coll Cardiol 2007; 50(23): 2207-2214.  Back to cited text no. 36
Bratincsák A, El-Said HG, Bradley JS, Shayan K, Grossfeld PD, Cannavino CR. Fulminant myocarditis associated with pandemic H1N1 influenza A virus in children. J Am Coll Cardiol 2010; 55(9): 928-929.  Back to cited text no. 37
Klein R, Jiang H, Niederacher D, Adams O, Du M, Horlitz M, et al. Frequency and quantity of the parvovirus B19 genome in endomyocardial biopsies from patients with suspected myocarditis or idiopathic left ventricular dysfunction. Z Kardiol 2004; 93(4): 300-309.  Back to cited text no. 38
Kühl U, Pauschinger M, Seeberg B, Lassner D, Noutsias M, Poller W, et al. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 2005; 112(13): 1965-1970.  Back to cited text no. 39
Matsumori A, Shimada T, Chapman NM, Tracy SM, Mason JW. Myocarditis and heart failure associated with hepatitis C virus infection. J Cardiac Fail 2006; 12(4): 293-298.  Back to cited text no. 40
Schönian U, Crombach M, Maser S, Maisch B. Cytomegalovirus- associated heart muscle disease. Eur Heart J 1995; 16(suppl_O): 46-49.  Back to cited text no. 41
Vallbracht KB, Schwimmbeck PL, Kühl U, Seeberg B, Schultheiss H-P. Endothelium-dependent flow-mediated vasodilation of systemic arteries is impaired in patients with myocardial virus persistence. Circulation 2004; 110(18): 2938-2945.  Back to cited text no. 42
Bachelier K, Biehl S, Schwarz V, Kindermann I, Kandolf R, Sauter M, et al. Parvovirus B19-induced vascular damage in the heart is associated with elevated circulating endothelial microparticles. PloS One 2017; 12(5): e0176311.  Back to cited text no. 43
Frustaci A, Chimenti C, Calabrese F, Pieroni M, Thiene G, Maseri A. Immunosuppressive therapy for active lymphocytic myocarditis: virological and immunologic profile of responders versus nonresponders. Circulation 2003; 107(6): 857-863.  Back to cited text no. 44
O’Neill D, McARTHUR JD, Kennedy JA, Clements G. Coxsackie B virus infection in coronary care unit patients. J Clin Pathol 1983; 36(6): 658-661.  Back to cited text no. 45
El-Hagrassy MO, Banatvala J, Coltart D. Coxsackie-B-virus-specific IgM responses in patients with cardiac and other diseases. Lancet 1980; 316(8205): 1160-1162.  Back to cited text no. 46
Nielsen TS, Hansen J, Nielsen LP, Baandrup UT, Banner J. The presence of enterovirus, adenovirus, and parvovirus B19 in myocardial tissue samples from autopsies: an evaluation of their frequencies in deceased individuals with myocarditis and in non-inflamed control hearts. Forensic Sci Medicine Pathol 2014; 10(3): 344-350.  Back to cited text no. 47
Pankuweit S, Moll R, Baandrup U, Portig I, Hufnagel G, Maisch B. Prevalence of the parvovirus B19 genome in endomyocardial biopsy specimens. Human Pathol 2003; 34(5): 497-503.  Back to cited text no. 48
Bock C-T, Klingel K, Kandolf R. Human parvovirus B19-associated myocarditis. New Engl J Med 2010; 362(13): 1248-1249.  Back to cited text no. 49
Bültmann BD, Klingel K, Näbauer M, Wallwiener D, Kandolf R. High prevalence of viral genomes and inflammation in peripartum cardiomyopathy. Am J Obstet Gynecol 2005; 193(2): 363-365.  Back to cited text no. 50
Martin AB, Webber S, Fricker FJ, Jaffe R, Demmler G, Kearney D, et al. Acute myocarditis. Rapid diagnosis by PCR in children. Circulation 1994; 90(1): 330-339.  Back to cited text no. 51
Savón C, Acosta B, Valdés O, Goyenechea A, Gonzalez G, Piñón A, et al. A myocarditis outbreak with fatal cases associated with adenovirus subgenera C among children from Havana City in 2005. J Clin Virol 2008; 43(2): 152-157.  Back to cited text no. 52
Camargo PR, Okay TS, Yamamoto L, Del Negro GMB, Lopes AA. Myocarditis in children and detection of viruses in myocardial tissue: implications for immunosuppressive therapy. Int J Cardiol 2011; 148(2): 204-208.  Back to cited text no. 53
Why HJF, Meany B, Richardson PJ, Olsen EGJ, Bowles NE, Cunningham L, et al. Clinical and prognostic significance of detection of enteroviral RNA in the myocardium of patients with myocarditis or dilated cardiomyopathy. Circulation 1994; 89(6): 2582-2589.  Back to cited text no. 54
Reibis R, Kühl U, Salzwedel A, Rasawieh M, Eichler S, Wegscheider K, et al. Return to work in heart failure patients with suspected viral myocarditis. SAGE Open Med 2017; 5: 2050312117744978.  Back to cited text no. 55
Ozdemir R, Kucuk M, Dibeklioglu SE. Report of a myocarditis outbreak among pediatric patients: human herpesvirus 7 as a causative agent? J Tropical Pediatr 2018; 64(6):468-471.  Back to cited text no. 56
Frustaci A, Francone M, Petrosillo N, Chimenti C. High prevalence of myocarditis in patients with hypertensive heart disease and cardiac deterioration. Eur J Heart Fail 2013; 15(3): 284-291.  Back to cited text no. 57
Mavrogeni S, Bratis K, Markussis V, Spargias C, Papadopoulou E, Papamentzelopoulos S, et al. The diagnostic role of cardiac magnetic resonance imaging in detecting myocardial inflammation in systemic lupus erythematosus. Differentiation from viral myocarditis. Lupus 2013; 22(1): 34-43.  Back to cited text no. 58
Jeserich M, Brunner E, Kandolf R, Olschewski M, Kimmel S, Friedrich MG, et al. Diagnosis of viral myocarditis by cardiac magnetic resonance and viral genome detection in peripheral blood. Int J Cardiovasc Imaging 2013; 29(1): 121-129.  Back to cited text no. 59
Koepsell SA, Anderson DR, Radio SJ. Parvovirus B19 is a bystander in adult myocarditis. Cardiovasc Pathol 2012; 21(6): 476-481.  Back to cited text no. 60
Mavrogeni S, Spargias C, Bratis C, Kolovou G, Markussis V, Papadopoulou E, et al. Myocarditis as a precipitating factor for heart failure: evaluation and 1-year follow-up using cardiovascular magnetic resonance and endomyocardial biopsy. Eur J Heart Fail 2011; 13(8): 830-837.  Back to cited text no. 61
Escher F, Modrow S, Sabi T, Kühl U, Lassner D, Schultheiss HP, et al. Parvovirus B19 profiles in patients presenting with acute myocarditis and chronic dilated cardiomyopathy. Med Sci Monit 2008; 14(12): CR589- CR97.  Back to cited text no. 62
Lindner J, Noutsias M, Lassner D, Wenzel J, Schultheiss H-P, Kuehl U, et al. Adaptive immune responses against parvovirus B19 in patients with myocardial disease. J Clin Virol 2009; 44(1): 27-32.  Back to cited text no. 63
Valdés O, Acosta B, Piñón A, Savón C, Goyenechea A, Gonzalez G, et al. First report on fatal myocarditis associated with adenovirus infection in Cuba. J Med Virol 2008; 80(10): 1756-1761.  Back to cited text no. 64
Carturan E, Milanesi O, Kato Y, Giacometti C, Biffanti R, Thiene G, et al. Viral detection and tumor necrosis factor alpha profile in tracheal aspirates from children with suspicion of myocarditis. Diagnost Mol Pathol 2008; 17(1): 21-27.  Back to cited text no. 65
Yilmaz A, Mahrholdt H, Athanasiadis A, Vogelsberg H, Meinhardt G, Voehringer M, et al. Coronary vasospasm as the underlying cause for chest pain in patients with PVB19-myocarditis. Heart 2008; 94(11): 1456-1463.  Back to cited text no. 66
Guarner J, Bhatnagar J, Shieh W-J, Nolte KB, Klein D, Gookin MS, et al. Histopathologic, immunohistochemical, and polymerase chain reaction assays in the study of cases with fatal sporadic myocarditis. Human Pathol 2007; 38(9): 1412-1419.  Back to cited text no. 67
Topkara VK, Dang NC, Barili F, Martens TP, George I, Cheema FH, et al. Ventricular assist device use for the treatment of acute viral myocarditis. J Thorac Cardiovasc Surg 2006; 131(5): 1190-1191.  Back to cited text no. 68
Amabile N, Fraisse A, Bouvenot J, Chetaille P, Ovaert C. Outcome of acute fulminant myocarditis in children. Heart 2006; 92(9): 1269-1273.  Back to cited text no. 69
Kytö V, Vuorinen T, Saukko P, Lautenschlager I, Lignitz E, Saraste A, et al. Cytomegalovirus infection of the heart is common in patients with fatal myocarditis. Clin Infect Dis 2005; 40(5): 683-688.  Back to cited text no. 70
English RF, Janosky JE, Ettedgui JA, Webber SA. Outcomes for children with acute myocarditis. Cardiol Young 2004; 14(5): 488-493.  Back to cited text no. 71
Zhang HY, Li Y, McClean DR, Richardson PJ, Florio R, Sheppard M, et al. Detection of enterovirus capsid protein VP1 in myocardium from cases of myocarditis or dilated cardiomyopathy by immunohistochemistry: further evidence of enterovirus persistence in myocytes. Med Microbiol Immunol 2004; 193(2-3): 109-114.  Back to cited text no. 72
Ali M, Abdel-Dayem T. Myocarditis: an expected health hazard associated with water resources contaminated with Coxsackie viruses type B. Int J Environ Health Res 2003; 13(3): 261-270.  Back to cited text no. 73
Satoh M, Nakamura M, Akatsu T, Iwasaka J, Shimoda Y, Segawa I, et al. Expression of Toll-like receptor 4 is associated with enteroviral replication in human myocarditis. Clin Sci 2003; 104(6): 577-584.  Back to cited text no. 74
Gut W, Wielkopolska A, Binduga-Gajewska I, Jarzabek Z. Evaluation of the usefulness of the ELISA method for detection of enterovirus antibodies in serum samples of patients with myocarditis. Med Sci Monit 2002; 8(1): MT10-MT4.  Back to cited text no. 75
Matsumori A, Yutani C, Ikeda Y, Kawai S, Sasayama S. Hepatitis C virus from the hearts of patients with myocarditis and cardiomyopathy. Lab Invest 2000; 80(7): 1137.  Back to cited text no. 76
Zhang HY, Li Y, Peng T, Aasa M, Zhang L, Yang Y, et al. Localization of enteroviral antigen in myocardium and other tissues from patients with heart muscle disease by an improved immunohistochemical technique. J Histochem Cytochem 2000; 48(5): 579-584.  Back to cited text no. 77
Bowles NE, Kearney DL, Ni J, Perez-Atayde AR, Kline MW, Bricker JT, et al. The detection of viral genomes by polymerase chain reaction in the myocardium of pediatric patients with advanced HIV disease. J Am Coll Cardiol 1999; 34(3): 857-865.  Back to cited text no. 78
Akhtar N, Ni J, Stromberg D, Rosenthal GL, Bowles NE, Towbin JA. Tracheal aspirate as a substrate for polymerase chain reaction detection of viral genome in childhood pneumonia and myocarditis. Circulation 1999; 99(15): 2011-2018.  Back to cited text no. 79
Grumbach IM, Heim A, Pring-Akerblom P, Vonhof S, Hein W, Müller G, et al. Adenoviruses and enteroviruses as pathogens in myocarditis and dilated cardiomyopathy. Acta Cardiolog 1999; 54(2): 83-88.  Back to cited text no. 80
Petitjean J, Kopecka H, Freymuth F, Langlard J, Scanu P, Galateau F, et al. Detection of enteroviruses in endomyocardial biopsy by molecular approach. J Med Virol 1992; 37(1): 76-82.  Back to cited text no. 81
Mariani M, Petronio AS, Manes MT, Morelli M, Squecco D, Nardini V, et al. Detection of enteroviral infection in myocardial tissues by polymerase chain reaction (PCR). Clin Microbiol Infect 1996; 2(2): 109114.  Back to cited text no. 82
Pauschinger M, Doerner A, Kuehl U, Schwimmbeck PL, Poller W, Kandolf R, Schultheiss HP, et al. Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 1999; 99(7): 889-895.  Back to cited text no. 83
Lv S, Rong J, Ren S, Wu M, Li M, Zhu Y, et al. Epidemiology and diagnosis of viral myocarditis. Hellenic J Cardiol 2013; 54(5): 382-391.  Back to cited text no. 84
Ellis CR, Di Salvo T. Myocarditis: basic and clinical aspects. Cardiol Rev 2007; 15(4): 170-177.  Back to cited text no. 85
[85]Magnani JW, Dec GW. Myocarditis: current trends in diagnosis and treatment. Circulation 2006; 113(6): 876-890.  Back to cited text no. 86
Kühl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, et al. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with “idiopathic” left ventricular dysfunction. Circulation 2005; 111: 887-893.  Back to cited text no. 87
Griffin LD, Kearney D, Ni J, Jaffe R, Fricker FJ, Webber S, et al. Analysis of formalin-fixed and frozen myocardial autopsy samples for viral genome in childhood myocarditis and dilated cardiomyopathy with endocardial fibroelastosis using polymerase chain reaction (PCR). Cardiovasc Pathol 1995; 4: 3-11.  Back to cited text no. 88


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]

  [Table 1]

This article has been cited by
1 Targeted treatment in viral-associated inflammatory cardiomyopathy
Ahmad Amin,Sepideh Taghavi,Maryam Chenaghlou,Elahe Zare,Monireh Kamali,Nasim Naderi
Clinical Case Reports. 2021; 9(7)
[Pubmed] | [DOI]
2 Association of parvovirus B19 and myocarditis/dilated cardiomyopathy: A systematic review and meta-analysis
Alireza Khatami, Mohammad Hossein Razizadeh, Monire Ghadirali, Shahrooz Yazdani, Saeed Bahadory, Alireza Soleimani
Microbial Pathogenesis. 2021; : 105207
[Pubmed] | [DOI]
3 Cardioprotective effects of omega 3 fatty acids from fish oil and it enhances autoimmunity in porcine cardiac myosin-induced myocarditis in the rat model
Ling-Yan Li,Xu Wang,Ting-Chuan Zhang,Zong-Jun Liu,Jun-Qing Gao
Zeitschrift für Naturforschung C. 2021; 0(0)
[Pubmed] | [DOI]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  2. Materials and...
  In this article
1. Introduction
3. Results
4. Discussion
Article Figures
Article Tables

 Article Access Statistics
    PDF Downloaded406    
    Comments [Add]    
    Cited by others 3    

Recommend this journal