Skip to main content
Top
Published in: Forensic Science, Medicine and Pathology 1/2010

01-03-2010 | Original Article

Sudden death related myocarditis: a study of 56 cases

Authors: Indira D. Kitulwatte, Patrick J. H. Kim, Michael S. Pollanen

Published in: Forensic Science, Medicine and Pathology | Issue 1/2010

Login to get access

Abstract

Fifty-six cases of sudden death from myocarditis were reviewed to characterize the range of histologic appearances of myocarditis. All autopsy cases of myocarditis over 13 years (1996–2008) in the Toronto Forensic Pathology Unit, Ontario Forensic Pathology Service, were studied. In each case, historical documentation and histological slides were reviewed. The severity of myocarditis was graded qualitatively and quantitatively (the inflammatory index). We established the inflammatory index in order to classify the severity of myocarditis, by counting the mean number of inflammatory foci per section of myocardium. Based on the inflammatory index, myocardial inflammation was classified into four grades. Based on this classification, 47% of the cases were classified as marked myocarditis having an inflammatory index over 5, with the number of foci per slide varying from 3 to more than 10, while 20% were classified as mild myocarditis with an inflammatory index between 1.1 and 1.9 with the number of foci per slide varying from 0 to 6. The diagnosis of mild myocarditis is dependent on adequate sampling. We believe that the use of this inflammatory index enhances the post-mortem diagnostic sensitivity of myocarditis, especially in its mild form and correlates with qualitative assessment of the histologic severity of myocarditis.
Literature
1.
go back to reference Mattingly TW. Changing concepts of myocardial diseases. JAMA. 1965;191:127–31. Mattingly TW. Changing concepts of myocardial diseases. JAMA. 1965;191:127–31.
2.
go back to reference Berry GJ, Atkins KA. Pathology of Human Myocarditis, Myocarditis: from Bench to Bedside. Clifton: Humana; 2002. p. 325–70. Berry GJ, Atkins KA. Pathology of Human Myocarditis, Myocarditis: from Bench to Bedside. Clifton: Humana; 2002. p. 325–70.
3.
go back to reference Okada R, Wakafuji S. Myocarditis in autopsy. Heart Vessels. 1985;1(suppl 1):23–9.CrossRef Okada R, Wakafuji S. Myocarditis in autopsy. Heart Vessels. 1985;1(suppl 1):23–9.CrossRef
4.
go back to reference Hoshikawa N, Shirasawa K, Kurata T. Four autopsy cases of acute viral myocarditis. Heart Vessels. 1985;1:165–6.CrossRef Hoshikawa N, Shirasawa K, Kurata T. Four autopsy cases of acute viral myocarditis. Heart Vessels. 1985;1:165–6.CrossRef
5.
go back to reference Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, Fenoglio JJ Jr, et al. Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol. 1986;1:3–14. Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, Fenoglio JJ Jr, et al. Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol. 1986;1:3–14.
6.
go back to reference Shanes JG, Ghali J, Billingham ME, Ferrans VJ, Fenoglio JJ, Edwards WD, et al. Interobserver variability in the pathologic interpretation of endomyocardialbiopsy results. Circulation. 1987;75:401–5.PubMed Shanes JG, Ghali J, Billingham ME, Ferrans VJ, Fenoglio JJ, Edwards WD, et al. Interobserver variability in the pathologic interpretation of endomyocardialbiopsy results. Circulation. 1987;75:401–5.PubMed
7.
go back to reference Magnani JW, Dec GW. Myocarditis; current trends in diagnosis and treatment. Circulation. 2006;113:876–90.CrossRefPubMed Magnani JW, Dec GW. Myocarditis; current trends in diagnosis and treatment. Circulation. 2006;113:876–90.CrossRefPubMed
9.
go back to reference Shirani J, Freant LJ, Robert WC. Gross and semiquantitative histologic findings in mononuclear cell myocarditis causing sudden death, and implications for endomyocardial biopsy. Am J Cardiol. 1993;72:952–67.CrossRefPubMed Shirani J, Freant LJ, Robert WC. Gross and semiquantitative histologic findings in mononuclear cell myocarditis causing sudden death, and implications for endomyocardial biopsy. Am J Cardiol. 1993;72:952–67.CrossRefPubMed
10.
go back to reference Edwards WD. Current problems in establishing quantitative histopathologic criteria for the diagnosis of lymphocytic myocarditis by endomyocardial biopsy. Heart Vessels. 1985;1(Suppl 1):138–42.CrossRef Edwards WD. Current problems in establishing quantitative histopathologic criteria for the diagnosis of lymphocytic myocarditis by endomyocardial biopsy. Heart Vessels. 1985;1(Suppl 1):138–42.CrossRef
12.
go back to reference Drory Y, Turetz Y, Hiss Y, et al. Sudden unexpected death in persons less than 40 years of age. Am J Cardiol. 1991;68:1388–92.CrossRefPubMed Drory Y, Turetz Y, Hiss Y, et al. Sudden unexpected death in persons less than 40 years of age. Am J Cardiol. 1991;68:1388–92.CrossRefPubMed
13.
go back to reference Weber MA, Ashworth MT, Risdon RA, Malone M, Burch M, Sebire NJ. Clinicopathological features of paediatric deaths due to myocarditis: an autopsy series. Arch Dis Child. 2008;93:594–8.CrossRefPubMed Weber MA, Ashworth MT, Risdon RA, Malone M, Burch M, Sebire NJ. Clinicopathological features of paediatric deaths due to myocarditis: an autopsy series. Arch Dis Child. 2008;93:594–8.CrossRefPubMed
14.
go back to reference Gupta S, Markham DW, Drazner MH, Mammen PPA. Fulminant myocarditis. Nat Clin Pract Cardiovasc Med. 2008;5(11):693–706.CrossRefPubMed Gupta S, Markham DW, Drazner MH, Mammen PPA. Fulminant myocarditis. Nat Clin Pract Cardiovasc Med. 2008;5(11):693–706.CrossRefPubMed
15.
go back to reference Woodruff JF. Viral myocarditis, a review. Am J Pathol. 1980;101(2):428–84. Woodruff JF. Viral myocarditis, a review. Am J Pathol. 1980;101(2):428–84.
17.
go back to reference Esfandiarei M, McManus BM. Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol Mech Dis. 2008;3:127–55.CrossRef Esfandiarei M, McManus BM. Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol Mech Dis. 2008;3:127–55.CrossRef
18.
go back to reference Mamas MA, Fraser D, Neyses L. Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol. 2008;130(3):304–9.CrossRefPubMed Mamas MA, Fraser D, Neyses L. Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol. 2008;130(3):304–9.CrossRefPubMed
19.
go back to reference Herskowitz A, Ahmed-Ansari A, Neumann DA, et al. Induction of major histocompatibility complex antigens within the myocardium of patients with active myocarditis: a nonhistologic marker of myocarditis. J Am Coll Cardiol. 1990;15:624–32.PubMed Herskowitz A, Ahmed-Ansari A, Neumann DA, et al. Induction of major histocompatibility complex antigens within the myocardium of patients with active myocarditis: a nonhistologic marker of myocarditis. J Am Coll Cardiol. 1990;15:624–32.PubMed
20.
go back to reference Maisch B, Portig I, Ristic A, Hufnagel G, Pankuweit S. Definition of inflammatory cardiomyopathy (myocarditis): on the way to consensus: a status report. Herz. 2000;25:200–9.CrossRefPubMed Maisch B, Portig I, Ristic A, Hufnagel G, Pankuweit S. Definition of inflammatory cardiomyopathy (myocarditis): on the way to consensus: a status report. Herz. 2000;25:200–9.CrossRefPubMed
21.
go back to reference Dettmeyer R, Reith K, Madea B. Alcoholic cardiomyopathy versus chronic myocarditis—immunohistological investigations with LCA, CD3, CD68 and tenascin. Forensic Sci Int. 2002;126(1):57–62.CrossRefPubMed Dettmeyer R, Reith K, Madea B. Alcoholic cardiomyopathy versus chronic myocarditis—immunohistological investigations with LCA, CD3, CD68 and tenascin. Forensic Sci Int. 2002;126(1):57–62.CrossRefPubMed
22.
go back to reference Dettmeyer R, Baasner A, Schlamann M, Padosch SA, Haag C, Kandolf R, et al. Role of virus-induced myocardial affections in sudden infant death syndrome: a prospective postmortem study. Pediatr Res. 2004;55(6):947–52.CrossRefPubMed Dettmeyer R, Baasner A, Schlamann M, Padosch SA, Haag C, Kandolf R, et al. Role of virus-induced myocardial affections in sudden infant death syndrome: a prospective postmortem study. Pediatr Res. 2004;55(6):947–52.CrossRefPubMed
23.
go back to reference Chow LH, Radio SJ, Sears TD, McManus BM. Insensitivity of right ventricular endomyocardial biopsy in the diagnosis of myocarditis. J Am Coll Cardiol. 1989;14:915–20.PubMedCrossRef Chow LH, Radio SJ, Sears TD, McManus BM. Insensitivity of right ventricular endomyocardial biopsy in the diagnosis of myocarditis. J Am Coll Cardiol. 1989;14:915–20.PubMedCrossRef
24.
go back to reference Hauck AJ, Kearney DL, Edwards WD. Evaluation of postmortem endomyocardial biopsy specimens from 38 patients with lymphocytic myocarditis: implications for role of sampling error. Mayo Clin Proc. 1989;64:1235–45.PubMed Hauck AJ, Kearney DL, Edwards WD. Evaluation of postmortem endomyocardial biopsy specimens from 38 patients with lymphocytic myocarditis: implications for role of sampling error. Mayo Clin Proc. 1989;64:1235–45.PubMed
25.
go back to reference Billingham ME. The diagnostic criteria of myocarditis by endomyocardial biopsy. Heart Vessels. 1985;1(suppl 1):133–7.CrossRef Billingham ME. The diagnostic criteria of myocarditis by endomyocardial biopsy. Heart Vessels. 1985;1(suppl 1):133–7.CrossRef
26.
go back to reference Edwards WD, Holmes DR Jr, Reeder GS. Diagnosis of active lymphocytic myocarditis by endomyocardial biopsy: quantitative criteria for light microscopy. Mayo Clin Proc. 1982;57:419–25.PubMed Edwards WD, Holmes DR Jr, Reeder GS. Diagnosis of active lymphocytic myocarditis by endomyocardial biopsy: quantitative criteria for light microscopy. Mayo Clin Proc. 1982;57:419–25.PubMed
28.
go back to reference Edwards WD. Myocarditis and endomyocardial biopsy. In: Waller BF, editor. Cardiology Clinics, vol 2, no 4. Philadelphia: Saunders; 1984. pp. 647–656. Edwards WD. Myocarditis and endomyocardial biopsy. In: Waller BF, editor. Cardiology Clinics, vol 2, no 4. Philadelphia: Saunders; 1984. pp. 647–656.
29.
go back to reference Baandrup U, Florio RA, Olsen EGJ. Do endomyocardial biopsies represent the morphology of the rest of the myocardium? A quantitative light microscopic study of single v. multiple biopsies with the King’s bioptome. Eur Heart J. 1982;3(2):171–8.PubMed Baandrup U, Florio RA, Olsen EGJ. Do endomyocardial biopsies represent the morphology of the rest of the myocardium? A quantitative light microscopic study of single v. multiple biopsies with the King’s bioptome. Eur Heart J. 1982;3(2):171–8.PubMed
30.
go back to reference Kaneshige T, Machida N, Nakao S, Doiguchiy O, Katsudaz S, Yamane Y. Complete atrioventricular block associated with lymphocytic myocarditis of the atrioventricular node in two young adult dogs. J Comp Path. 2007;137:146–50.CrossRefPubMed Kaneshige T, Machida N, Nakao S, Doiguchiy O, Katsudaz S, Yamane Y. Complete atrioventricular block associated with lymphocytic myocarditis of the atrioventricular node in two young adult dogs. J Comp Path. 2007;137:146–50.CrossRefPubMed
31.
go back to reference Strauss DG, Katherine C. Imaging myocardial scar and arrhythmic risk prediction—a role for the electrocardiogram? J Electrocardiol. 2009;42:138.e1–8.CrossRef Strauss DG, Katherine C. Imaging myocardial scar and arrhythmic risk prediction—a role for the electrocardiogram? J Electrocardiol. 2009;42:138.e1–8.CrossRef
32.
go back to reference Stevens PJ, Ground KE. Occurrence and significance of myocarditis in trauma. Aerosp Med. 1970;41:770–80. Stevens PJ, Ground KE. Occurrence and significance of myocarditis in trauma. Aerosp Med. 1970;41:770–80.
33.
go back to reference Krous HF, et al. Myocardial inflammation, cellular death, and viral detection in sudden infant death caused by SIDS, suffocation, or myocarditis. Pediatr Res. 2009;66(1):17–21.CrossRefPubMed Krous HF, et al. Myocardial inflammation, cellular death, and viral detection in sudden infant death caused by SIDS, suffocation, or myocarditis. Pediatr Res. 2009;66(1):17–21.CrossRefPubMed
34.
go back to reference Berry GJ, Atkins KA. Pathology of human myocarditis. In: Cooper Jr. LT, editor. Myocarditis from bench to bedside. Clifton: Humana; 2003. pp. 325–370 (621 pp, illustrated. Totowa NJ). Berry GJ, Atkins KA. Pathology of human myocarditis. In: Cooper Jr. LT, editor. Myocarditis from bench to bedside. Clifton: Humana; 2003. pp. 325–370 (621 pp, illustrated. Totowa NJ).
35.
go back to reference Gravanis MB, Sternby NH. Incidence of myocarditis. A 10-year autopsy study from Malmo, Sweden. Arch Pathol Lab Med. 1991;115:390–2.PubMed Gravanis MB, Sternby NH. Incidence of myocarditis. A 10-year autopsy study from Malmo, Sweden. Arch Pathol Lab Med. 1991;115:390–2.PubMed
36.
go back to reference Kyto V, Saukko P, Lignitz E, Schwesinger G, Henn V, Saraste A, et al. Diagnosis and presentation of fatal myocarditis. Hum Pathol. 2005;36:1003–7.CrossRefPubMed Kyto V, Saukko P, Lignitz E, Schwesinger G, Henn V, Saraste A, et al. Diagnosis and presentation of fatal myocarditis. Hum Pathol. 2005;36:1003–7.CrossRefPubMed
37.
go back to reference Nolte KB, Alakija P, Oty G, Shaw MW, Subbarao K, Guarner J, et al. Influenza A virus infection complicated by fatal myocarditis. Am J Forensic Med Pathol. 2000;21(4):375–9.CrossRefPubMed Nolte KB, Alakija P, Oty G, Shaw MW, Subbarao K, Guarner J, et al. Influenza A virus infection complicated by fatal myocarditis. Am J Forensic Med Pathol. 2000;21(4):375–9.CrossRefPubMed
38.
go back to reference Haddad F, Berry G, Doyle RL, Martineau P, Leung T-K, Racine N. Active bacterial myocarditis: a case report and review of the literature. J Heart Lung Transplant. 2007;26:745–9.CrossRefPubMed Haddad F, Berry G, Doyle RL, Martineau P, Leung T-K, Racine N. Active bacterial myocarditis: a case report and review of the literature. J Heart Lung Transplant. 2007;26:745–9.CrossRefPubMed
39.
go back to reference Foley DA, Edwards WD. Quantitation of leukocytes in endomyocardial tissue from 100 normal human hearts at autopsy. Implications for diagnosis of myocarditis from biopsy specimens of living patients. Am J Cardiovasc Pathol. 1988;2(2):145–9.PubMed Foley DA, Edwards WD. Quantitation of leukocytes in endomyocardial tissue from 100 normal human hearts at autopsy. Implications for diagnosis of myocarditis from biopsy specimens of living patients. Am J Cardiovasc Pathol. 1988;2(2):145–9.PubMed
40.
go back to reference Cooper LT, Berry GJ, Shabetai R. Idiopathic giant-cell myocarditis—natural history and treatment. N Engl J Med. 1997;336(26):1860–6.CrossRefPubMed Cooper LT, Berry GJ, Shabetai R. Idiopathic giant-cell myocarditis—natural history and treatment. N Engl J Med. 1997;336(26):1860–6.CrossRefPubMed
41.
go back to reference Billingham M, Tazelaar H. The morphological progression of viral myocarditis. Postgrad Med J. 1986;62:581–4.CrossRefPubMed Billingham M, Tazelaar H. The morphological progression of viral myocarditis. Postgrad Med J. 1986;62:581–4.CrossRefPubMed
42.
go back to reference Keogh AM, Billingham ME, Schroeder JS. Rapid histological. Changes-in endomyocardial biopsy specimens after myocarditis. Br Heart J. 1990;64:406–8.CrossRefPubMed Keogh AM, Billingham ME, Schroeder JS. Rapid histological. Changes-in endomyocardial biopsy specimens after myocarditis. Br Heart J. 1990;64:406–8.CrossRefPubMed
43.
go back to reference Babu-Narayan SV, McCarthy KP, Ho SY, Magee AG, Kilner PJ, Sheppard MN. Myocarditis and sudden cardiac death in the young extensive fibrosis suggested by cardiovascular magnetic resonance in vivo and confirmed post mortem. Circulation. 2007;116:e122–5.CrossRefPubMed Babu-Narayan SV, McCarthy KP, Ho SY, Magee AG, Kilner PJ, Sheppard MN. Myocarditis and sudden cardiac death in the young extensive fibrosis suggested by cardiovascular magnetic resonance in vivo and confirmed post mortem. Circulation. 2007;116:e122–5.CrossRefPubMed
44.
go back to reference Lecomte D, Fornes P, Fouret P, Nicolas G. Isolated myocardial fibrosis as a cause of sudden cardiac death and its possible relation to myocarditis. J Forensic Sci. 1993;38(3):617–21.PubMed Lecomte D, Fornes P, Fouret P, Nicolas G. Isolated myocardial fibrosis as a cause of sudden cardiac death and its possible relation to myocarditis. J Forensic Sci. 1993;38(3):617–21.PubMed
45.
go back to reference Wassmuth R, Schulz-Menger J. Cardiac magnetic resonance in acute myocarditis and dilated cardiomyopathy. Med Sci Monit. 2009;15(5):RA111–9.PubMed Wassmuth R, Schulz-Menger J. Cardiac magnetic resonance in acute myocarditis and dilated cardiomyopathy. Med Sci Monit. 2009;15(5):RA111–9.PubMed
46.
go back to reference Bohl S, Wassmuth R, Abdel-Aty H, Rudolph A, Messroghli D, Dietz R, et al. Delayed enhancement cardiac magnetic resonance imaging reveals typical patterns of myocardial injury in patients with various forms of non-ischemic heart disease. Int J Cardiovasc Imaging. 2008;24:597–607.CrossRefPubMed Bohl S, Wassmuth R, Abdel-Aty H, Rudolph A, Messroghli D, Dietz R, et al. Delayed enhancement cardiac magnetic resonance imaging reveals typical patterns of myocardial injury in patients with various forms of non-ischemic heart disease. Int J Cardiovasc Imaging. 2008;24:597–607.CrossRefPubMed
47.
go back to reference Postan M, Cheever AW, Dvorak JA, Mcdaniel JP. A histopathological analysis of the course of myocarditis in C3H/He mice infected with Trypanosoma cruzi clone Sylvio-X10/4. Trans R Soc Tropicaml Medicinea and Hygiene. 1986;80:50–5.CrossRef Postan M, Cheever AW, Dvorak JA, Mcdaniel JP. A histopathological analysis of the course of myocarditis in C3H/He mice infected with Trypanosoma cruzi clone Sylvio-X10/4. Trans R Soc Tropicaml Medicinea and Hygiene. 1986;80:50–5.CrossRef
48.
go back to reference De Cobelli F, Pieroni M, Esposito A, Chimenti C, Belloni E, Mellone R, et al. Delayed gadolinium-enhanced cardiac magnetic resonance in patients with chronic myocarditis presenting with heart failure or recurrent arrhythmias. J Am Coll Cardiol. 2006;47(8):1649–54.CrossRefPubMed De Cobelli F, Pieroni M, Esposito A, Chimenti C, Belloni E, Mellone R, et al. Delayed gadolinium-enhanced cardiac magnetic resonance in patients with chronic myocarditis presenting with heart failure or recurrent arrhythmias. J Am Coll Cardiol. 2006;47(8):1649–54.CrossRefPubMed
Metadata
Title
Sudden death related myocarditis: a study of 56 cases
Authors
Indira D. Kitulwatte
Patrick J. H. Kim
Michael S. Pollanen
Publication date
01-03-2010
Publisher
Humana Press Inc
Published in
Forensic Science, Medicine and Pathology / Issue 1/2010
Print ISSN: 1547-769X
Electronic ISSN: 1556-2891
DOI
https://doi.org/10.1007/s12024-009-9125-5

Other articles of this Issue 1/2010

Forensic Science, Medicine and Pathology 1/2010 Go to the issue

What's New Beyond Forensics

What’s new beyond forensics?