Distribution of biventricular disease in arrhythmogenic cardiomyopathy: an autopsy study
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1 Human Pathology (2012) 43, Original contribution Distribution of biventricular disease in arrhythmogenic cardiomyopathy: an autopsy study Fabio Tavora MD a, Mingchang Zhang MD b,c, Marcello Franco MD, PhD a, Joao Bosco Oliveira MD, PhD c, Ling Li MD d, David Fowler MD d, Ziqin Zhao MD b, Nathaniel Cresswell MS d, Allen Burke MD d, a Department of Pathology, Escola Paulista de Medicina, UNIFESP, Sao Paulo , Brazil b Department of Forensic Medicine, Shanghai Medical College, Fudan University, Shanghai , China c Department of Laboratory Medicine, National Institutes of Health, Bethesda, MD 20892, USA d University of Maryland Medical Center, Baltimore, MD 21201, USA Received 5 May 2011; revised 8 June 2011; accepted 10 June 2011 Keywords: Arrhythmia; Right ventricular cardiomyopathy; Sudden death; Myocarditis Summary Arrhythmogenic cardiomyopathy is a rare cardiomyopathy characterized by fibrofatty replacement primarily of the right ventricular myocardium. It is a major cause of sudden death in the young and in athletes. There are few autopsy studies of the ventricular distribution of the disease. Fifty cases of sudden cardiac death with fibrofatty replacement in either ventricle from a single medical examiner's office were studied. Distribution of disease as determined grossly and microscopically was correlated with activity at time of death, race, and presence of inflammation. Extent of disease was right ventricular in 6 cases (12%; age, 25 ± 5 years), biventricular in 25 (50%; age, 36 ± 3 years), and left ventricular in 19 (38%; age, 37 ± 3 years) (P =.13). Inflammation was present in 44% of biventricular arrhythmogenic cardiomyopathy versus 74% of left ventricular arrhythmogenic cardiomyopathy and 83% of right ventricular arrhythmogenic cardiomyopathy (P =.06). Arrhythmogenic cardiomyopathy, when presenting with sudden death, is usually biventricular. There is a trend that univentricular involvement occurs at an earlier age and that right ventricular involvement shows more inflammation, suggesting different stages of disease Elsevier Inc. All rights reserved. 1. Introduction Arrhythmogenic cardiomyopathy (AC) or its synonym arrhythmogenic right ventricular cardiomyopathy (ARVC) is a rare heart muscle disease in which the right ventricle is replaced by fibrofatty tissue [1]. ARVC is clinically characterized by ventricular tachyarrhythmias originating Corresponding author. Department of Pathology, University of Maryland, Baltimore, MD 21201, USA. address: allen.burke@gmail.com (A. Burke). from the right ventricle and by syncopal episodes and sudden death, which are often triggered by exercise. Pathologically, AC is characterized by fibrofatty replacement of the myocardium, accompanied by vacuolated myocytes and interstitial fibrosis. Inflammatory infiltrates have been reported in several cases, raising the possibility that AC is a form of healed myocarditis [1-5]. Although right ventricular disease formed the basis for the initial reports of AC, left ventricular involvement has been reported with increased frequency, and in some individuals, there may be a global dilated cardiomyopathy [6]. Recently, ARVC has /$ see front matter 2012 Elsevier Inc. All rights reserved. doi: /j.humpath
2 Distribution of biventricular disease in arrhythmogenic cardiomyopathy 593 been classified based on magnetic resonance imaging as classic (right ventricular predominant) in 39%, biventricular in 56%, and left dominant disease in 5% of patients [7]. There have been several autopsy studies of ARVC [4,8-11], one of which emphasized left ventricular involvement [8]. We herein characterize a series of ARVC from a single medical examiner's office to study the ventricular distribution of ARVC and correlate ventricular distribution with clinicopathologic parameters. 2. Materials and methods Fifty cases of sudden cardiac death with the diagnosis of ARVC were retrospectively studied. The disease was defined as subepicardial or right ventricular fibrofatty change surrounding altered degenerating cardiomyocytes. All cases were autopsied at the Office of the Chief Medical Examiner, Baltimore, MD, and were seen in consultation by cardiovascular pathologist and examined in a similar fashion. In all cases, autopsy reports were available, and full autopsy disclosed no other causes of death. Full-thickness sections of anterior, lateral, and posterior left ventricle; interventricular septum; and posterior and mid right ventricle were examined in every case. Distribution of disease was determined both grossly and microscopically, correlated with activity at time of death, race, and presence of inflammation. Inflammation was defined as 1 or more aggregate of lymphocytes, with 20 or more lymphocytes per aggregate. Cardiomegaly was defined based on established criteria depending on body weight [12]. 3. Results The mean age of the 50 subjects at the time of sudden death was 35.2 ± 15.7 years (Table 1). There were 23 whites (44%), 25 blacks (50%), and 2 Asians (4%). Death was exertional in 28 cases (56%). In only 3 cases did the autopsy report mention familial cardiac sudden death or cardiomyopathy. One patient had thyroiditis clinically and substantiated at autopsy, and one had a history of Alport syndrome. Heart weight was increased in 52% of the cases (range, g; mean, 438 g) with no difference among cases with left, right, or biventricular distribution of disease (P=0.1). Grossly, scar or fat replacement was seen in 26 (52%) in the right ventricle and 39 (78%) in the left ventricle (Fig. 1). Microscopically, scar or fat replacement was seen in 43 (86%) in the right ventricle and 45 (90%) in the left ventricle (Figs. 1 and 2). In cases of microscopic left ventricular involvement, 71% were patchy, 27% were circumferential, and 2% were apical; 91% showed fibrous tissue and fat, generally with a predominance of fibrous tissue; 9% showed only scar. The mean age of patients with circumferential left ventricular disease was 28 ± 9 years, compared with 39 ± 14 years for focal disease (P =.03). The anterior left ventricle was involved in 54%; lateral wall, in 86%; posterior wall, in 89%; and septum, in 43%. In the right ventricle, there was generally a higher amount of fat than fibrosis, although the distinction was complicated by the normal presence of fat in the right ventricular wall (Table 2). Extent of disease was predominantly right ventricular in 6 (12%; age, 25 ± 5 years), biventricular in 25 (50%; age, 36 ± 3 years), and left ventricular in 19 (38%; age, 37 ± 3 years) (Table 1). Seven cases (14%) had left ventricular involvement only, both gross and microscopically. The proportion of exertional deaths was greatest in right ventricular AC (83%) followed by left ventricular AC (64.7%) and biventricular (48%) (Table 2). Inflammation was present in 44% of biventricular AC versus 74% of left ventricular AC and 83% of right ventricular AC (P =.06). 4. Discussion The current study shows that the left ventricle is more frequently involved than the right in autopsy cases of AC. This finding has implications in the autopsy diagnosis of AC, in that medical examiners and pathologists who typically encounter sudden cardiac death need to be aware that left ventricular disease is not only common but may also be the only manifestation of AC. Only slightly more than half of hearts shows gross findings in the right ventricle. There may have been a selection bias to cases that come to the attention of the medical examiner's office, with sudden death cases without prior diagnosis more likely to be diagnosed only at autopsy. The need for microscopic sampling of the right ventricle in cases of suspected AC has been previously documented [13]. Although initially considered a right ventricular disease, AC is now known to involve both ventricles [3,14-21]. Webb Table 1 Distribution of clinical findings, by ventricular distribution Distribution Age (y) Male:female White:black:Asian Exertional (%) Biventricular 40 ± 15 22:3 11:13:1 50 Left ventricular 36 ± 12 16:3 9:9:1 58 Right ventricular 25 ± 11 5:1 3:3 83 P value
3 594 F. Tavora et al. Fig. 1 Biventricular disease in AC. A, Posterior right ventricle demonstrating area of thinning (arrow). B, Histologic section of area shown in A. There is haphazard replacement of the ventricular wall with fat and fibrosis. C, Posterolateral left ventricle with subepicardial fibrofatty replacement (arrows). D, Histologic section of area shown in C, showing patchy fatty replacement. et al [21] identified left ventricular dilatation or wall motion abnormalities in patients with ARVC by radionuclide angiography or cardiac catheterization, before the advent of cardiac magnetic resonance imaging. Autopsy studies have documented left ventricular fibrofatty infiltration in ARVC [5,15,19,22], and in some cases, the left ventricular involvement was extensive [15,19]. Only since the development and refinement of cardiac magnetic resonance imaging has the extent of fibrofatty replacement in ARVC been possible during life, with the use of delayed enhancement techniques with contrast [2,23]. A recent study of families has demonstrated the prevalence of left ventricular involvement in 84% of cases [7], which is very similar to the 78% rate of gross left ventricular involvement in the current study. By microscopic examination, the current study showed, as would be expected, an even higher rate of involvement. Although the subepicardial distribution of left ventricular scars in AC has been recognized at autopsy for several years, only recently has this distribution been appreciated by cardiac magnetic resonance imaging [7]. The close similarity between the ventricular distribution in the current autopsy study and clinical imaging studies is remarkable, in that familial cases were essentially absent in the current study, whereas a high proportion of patients with AC are recruited by family studies. Although only 3 patients in the current study had a family history, the number is likely significantly higher, given that detailed history was not always available. Also of interest is the high rate of African Americans in the current study, which is caused by the demographics of this particular medical examiner's system. AC is one of the major causes of sudden death worldwide, especially in Europe. Death is generally caused by ventricular tachycardia, with an onset most frequent in early adulthood [9]. Approximately 3 quarters of sudden deaths are exertional [9]; in the current study, slightly more than one half were. The current study confirms the marked male predisposition for AC. The mean age at death was higher in the current study than other series possibly because left and biventricular disease, which is more recently recognized, was seen in older individuals. In contrast, right ventricular AC (ARVC)
4 Distribution of biventricular disease in arrhythmogenic cardiomyopathy 595 Fig. 2 A and B, Fibrofatty infiltration of right ventricle. Epicardium is above. C and D, Fibrofatty infiltration of left ventricle. In D, there is a spared zone near the epicardium, although the fibrofatty change is predominantly subepicardial. B, C and D, Masson trichrome (original magnification 40). occurred in younger individuals. Against the concept that degree of disease correlates with stages or progression, we found that sudden death victims with extensive circumferential left ventricular involvement were actually younger than those with only focal involvement. The current study also showed that there was more inflammation in right ventricular disease than left ventricular AC, although of statistically borderline significance. It has been appreciated for many years that there is an inflammatory component in AC [1,3,4,10,24], which may or may not be integral to the pathogenesis of the disease. In conclusion, the current study demonstrates that ventricular distribution in AC is typically biventricular, with left ventricular involvement in the rule. The most Table 2 common locations of left ventricular involvement are the posterolateral walls in a subepicardial distribution, which is similar to that found in cardiac magnetic resonance studies. There were no significant differences in clinical presentation or histologic findings among subgroups, although the proportion of exertional deaths was greatest in right ventricular AC, and inflammation was more frequent. References [1] Thiene G, Corrado D, Basso C. Arrhythmogenic right ventricular cardiomyopathy/dysplasia. Orphanet J Rare Dis 2007;2:45. Pathologic parameters by subtype Biventricular Left ventricular Right ventricular P value Heart weight Cardiomegaly (%) RV gross (%) LV gross (%) Inflammation (%) 451 ± ± ± NA (b.0001) NA (b.0001)
5 596 F. Tavora et al. [2] Sen-Chowdhry S, Syrris P, Prasad SK, et al. Left-dominant arrhythmogenic cardiomyopathy: an under-recognized clinical entity. J Am Coll Cardiol 2008;52: [3] Suzuki H, Sumiyoshi M, Kawai S, et al. Arrhythmogenic right ventricular cardiomyopathy with an initial manifestation of severe left ventricular impairment and normal contraction of the right ventricle. Jpn Circ J 2000;64: [4] Burke AP, Farb A, Tashko G, Virmani R. Arrhythmogenic right ventricular cardiomyopathy and fatty replacement of the right ventricular myocardium: are they different diseases? Circulation 1998;97: [5] Sugrue DD, Edwards WD, Olney BA. Histologic abnormalities of the left ventricle in a patient with arrhythmogenic right ventricular dysplasia. Heart Vessels 1985;1: [6] Sen-Chowdhry S, Lowe MD, Sporton SC, McKenna WJ. Arrhythmogenic right ventricular cardiomyopathy: clinical presentation, diagnosis, and management. Am J Med 2004;117: [7] Sen-Chowdhry S, Syrris P, Ward D, Asimaki A, Sevdalis E, McKenna WJ. Clinical and genetic characterization of families with arrhythmogenic right ventricular dysplasia/cardiomyopathy provides novel insights into patterns of disease expression. Circulation 2007;115: [8] Lobo FV, Heggtveit HA, Butany J, Silver MD, Edwards JE. Right ventricular dysplasia: morphological findings in 13 cases. Can J Cardiol 1992;8: [9] Thiene G, Nava A, Corrado D, Rossi L, Pennelli N. Right ventricular cardiomyopathy and sudden death in young people. N Engl J Med 1988;318: [10] d'amati G, Leone O, di Gioia CR, et al. Arrhythmogenic right ventricular cardiomyopathy: clinicopathologic correlation based on a revised definition of pathologic patterns. HUM PATHOL 2001;32: [11] Fornes P, Ratel S, Lecomte D. Pathology of arrhythmogenic right ventricular cardiomyopathy/dysplasia an autopsy study of 20 forensic cases. J Forensic Sci 1998;43: [12] Kitzman DW, Scholz DG, Hagen PT, Ilstrup DM, Edwards WD. Agerelated changes in normal human hearts during the first 10 decades of life. Part II (maturity): a quantitative anatomic study of 765 specimens from subjects 20 to 99 years old. Mayo Clin Proc 1988;63: [13] Burke AP, Robinson S, Radentz S, Smialek J, Virmani R. Sudden death in right ventricular dysplasia with minimal gross abnormalities. J Forensic Sci 1999;44: [14] De Pasquale CG, Heddle WF. Left sided arrhythmogenic ventricular dysplasia in siblings. Heart 2001;86: [15] Gallo P, d'amati G, Pelliccia F. Pathologic evidence of extensive left ventricular involvement in arrhythmogenic right ventricular cardiomyopathy. HUM PATHOL 1992;23: [16] Lindstrom L, Nylander E, Larsson H, Wranne B. Left ventricular involvement in arrhythmogenic right ventricular cardiomyopathy a scintigraphic and echocardiographic study. Clin Physiol Funct Imaging 2005;25: [17] Lobo FV, Silver MD, Butany J, Heggtveit HA. Left ventricular involvement in right ventricular dysplasia/cardiomyopathy. Can J Cardiol 1999;15: [18] Michalodimitrakis M, Papadomanolakis A, Stiakakis J, Kanaki K. Left side right ventricular cardiomyopathy. Med Sci Law 2002;42: [19] Shoji T, Kaneko M, Onodera K, et al. Arrhythmogenic right ventricular dysplasia with massive involvement of the left ventricle. Can J Cardiol 1991;7: [20] Shrapnel M, Gilbert JD, Byard RW. Arrhythmogenic left ventricular dysplasia' and sudden death. Med Sci Law 2001;41: [21] Webb JG, Kerr CR, Huckell VF, Mizgala HF, Ricci DR. Left ventricular abnormalities in arrhythmogenic right ventricular dysplasia. Am J Cardiol 1986;58: [22] Saito K, Kuroda A, Arima S, Kawataki M, Tanaka H. Arrhythmogenic right ventricular dysplasia with left ventricular involvement: report of a case. Heart Vessels Suppl 1990;5:62-4. [23] Fogel MA, Weinberg PM, Harris M, Rhodes L. Usefulness of magnetic resonance imaging for the diagnosis of right ventricular dysplasia in children. Am J Cardiol 2006;97: [24] Basso C, Thiene G, Corrado D, Angelini A, Nava A, Valente M. Arrhythmogenic right ventricular cardiomyopathy. Dysplasia, dystrophy, or myocarditis. Circulation 1996;94:
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