(Circulation. 2001;103:269.)
© 2001 American Heart Association, Inc.
Clinical Investigation and Reports |
Ventricular Preexcitation in Children and Young Adults
Atrial Myocarditis as a Possible Trigger of Sudden Death
Presented in part at the 72nd Scientific Sessions of the American Heart Association, Atlanta, Ga, November 7–10, 1999.
From the Departments of Pathology (C.B., L.R., G.T.) and Cardiology (D.C.), University of Padua Medical School, Padua, Italy.
Correspondence to Gaetano Thiene, MD, FESC, FEACTS, Istituto di Anatomia Patologica, Via A. Gabelli 61, 35121 Padova, Italy. E-mail cardpath{at}ux1.unipd.it
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Abstract |
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Background—Sudden death (SD) in ventricular preexcitation (VP) syndrome is believed to be the result of atrial fibrillation with rapid ventricular response over the accessory pathway. Previous reports are anecdotal and often lack autopsy validation.
Methods and
Results—Prevalence and clinicopathological
features of VP were investigated in a series of 273 SDs in children and
young adults (aged 
35 years). Site of accessory atrioventricular (AV)
connection was predicted by 12-lead ECG. Right and left AV ring
together with the sinoatrial and AV septal junction were studied in
serial histological sections. Ten patients (3.6%; male, mean age 24±7
years) had VP: 8 had Wolff-Parkinson-White (WPW) and 2 had
Lown-Ganong-Levine (LGL) syndrome. Six patients had previous symptoms,
and SD occurred at rest in all but 1. Pathological substrates of LGL
consisted of AV-node hypoplasia and right-sided atrio-Hisian tract,
respectively. In the 8 WPW patients, 10 total accessory AV pathways
consisting of ordinary myocardium were found (7 left lateral, 2 right
posterolateral, and 1 septal). These pathways were close to the
endocardium (mean distance, 750±530 µm) and 310±190 µm thick. In
4 WPW patients (50%), isolated acute atrial myocarditis was found,
which was polymorphous in 1 and lymphocytic in
3.
Conclusions—VP accounted for 3.6% of SD in young people and was not preceded by warning symptoms in 40%. A left accessory pathway was the most frequent substrate, and its subendocardial location supports the feasibility of catheter ablation. Isolated atrial myocarditis may act as a trigger of paroxysmal atrial fibrillation that leads to SD.
Key Words: atrium • death, sudden • myocarditis • pathology • Wolff-Parkinson-White syndrome
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Introduction |
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Sudden death (SD) in ventricular preexcitation (VP) syndrome, although rare,1 2 3 arouses a great deal of interest because it often occurs in young, otherwise healthy individuals. In most cases, SD is the result of rapid ventricular response over the accessory pathway of atrial fibrillation, which might be triggered by a primary atrial pathology or be secondary to atrioventricular (AV) reentrant tachycardia.2 4
When one considers that histological confirmation of accessory pathways may require expert preparation and scrutiny of thousands of sections, it is not surprising that pathology lags far behind clinical studies. Thus, previous reports on SD patients are anecdotal and often lack autopsy validation; likewise, no data are available on VP as a cause of SD in the young. The present study was undertaken to assess prevalence and clinicopathological features of VP in a series of young adults who died suddenly.
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Methods |
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Since 1979, a clinicopathological prospective study of SD in children and young adults (
35 years) has been ongoing in
Northeastern Italy. All hearts from cases of SD are systematically
assessed at the University of Padua. Distribution of various causes of
SD has been previously
reported.5
For inclusion in the study group, each patient fulfilled the
following criteria: (1) ECG diagnosis of VP; (2) 35 years of age at
time of death; (3) absence at autopsy of other cardiac and noncardiac
causes of death; and (4) no evidence of drug or alcohol abuse on the
postmortem toxicological examination.
Clinical history was reviewed, and particular attention was paid to previous symptoms or signs, electrophysiological investigation, and circumstances of death.
Wolff-Parkinson-White (WPW)–type VP was diagnosed by
12-lead ECG in the presence of short PR interval (0.12 s) and
widening of the QRS complex (>0.12 s) with slurred, slow rising onset
of QRS (so-called 
-wave). The site of AV connection was predicted
according to ECG criteria of Arruda et
al6 (ie, -wave axis in the
frontal leads and -wave polarity in the precordial
leads).
Lown-Ganong-Levine (LGL)–type VP or enhanced AV nodal
conduction was diagnosed by 12-lead ECG in the presence of short PR
interval (0.12 s) and normal QRS complex (0.12 s).
Gross examination of the heart addressed weight, wall thickness, myocardium, endocardium, valves and coronary arteries, inflow and outflow tracts and great vessels.
Routine histology of the ordinary myocardium (stained with hematoxylin-eosin and Heidenhain trichrome) was performed on 8 transmural samples obtained in cross section from the left ventricle (anterior, lateral, and posterior), interventricular septum (anteroseptal, medioseptal, and posteroseptal) and right ventricle (anterior and posterior). Additionally, 8 myocardial samples were taken from right and left atrial free walls, including myocardium surrounding the ostium of the pulmonary veins.
In the setting of inflammatory infiltrates, to characterize the cell population, paraffin sections were stained with a panel of antibodies: CD45 (leukocyte common antigen), CD43 (T-lymphocytes), CD45RO (activated T-lymphocytes), CD20 (B-lymphocytes), CD4 (T-helpers), CD8 (cytotoxic T-lymphocytes), CD68 (macrophages), and CD31 (endothelium) (all from Dako), according to the avidin-biotin-peroxidase complex method (Vector).
After exclusion of extracardiac or other cardiac causes of SD by thorough gross and histological investigation, 2 blocks comprehensive of the sinoatrial and AV septal junctions (including AV node, His bundle, and bundle branches) were studied by serial sections technique according to Rossi.7 Blocks of lateral AV rings included atrial and ventricular myocardium and were cut serially as well. Entire blocks were fixed in 10% buffered formalin, embedded in paraffin, and serially sectioned at 7-µm intervals. At every tenth section, 1 section was stained with hematoxylin-eosin and the next consecutive section with Heidenhain trichrome. The remaining sections were studied, when necessary, after examination of the initially mounted series.
In the setting of accessory pathways, mean thickness and distance from the endocardium, epicardium, and coronary sinus (left lateral accessory pathways) were calculated by a micrometer; values were expressed in microns.
The conduction system as well as lateral AV rings were studied in serial sections in 10 young subjects (males; mean age, 24 years) who died from noncardiovascular causes and served as controls.
Statistical Analysis
Continuous variables are expressed as mean±SD.
2 or Fisher’s exact test was used to
assess significance of differences between subgroups. A 2-tailed
probability value <0.05 was regarded as statistically
significant.
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Results |
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Clinical Data
The 12-lead ECG tracing was available in 93 of 273 cardiovascular SDs (34%), and 10 patients had ECG-documented VP (3.6% of the overall SD population and 10.5% of SDs with available ECG). Six percent of all SDs remained unexplained even after careful gross and histological examination.
VP patients were male (mean age, 24±7 years; age range, 9 to 35 years). Six patients (60%) had warning symptoms that consisted of palpitations; these symptoms were associated with syncope in 3 of the 6. The remaining 4 patients had an incidental ECG diagnosis at military service preenrollment screening (n=2), preparticipation screening for sport activity (n=1), and checkup before surgical procedure (n=1). SD occurred at rest in all but 1; 4 died during night sleep.
The 12-lead ECG tracing indicated WPW-type VP in 8 patients
and enhanced AV conduction (LGL type) in 2. In the former, -wave
morphology suggested left lateral AV pathways in 6 (75%;
posterolateral in 3 and lateral in 3), and right AV accessory pathways
in 2 (posterolateral and lateral, 1 each); in 1 patient (patient 10),
the 12-lead ECG tracing intermittently showed -wave pattern (left
lateral) or a normal QRS pattern without VP
(Table 1
).
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Recurrent episodes of AV-reentrant tachycardia were reported in 5 patients (patients 2, 3, 6, 8, and 9). Electrophysiological study was undertaken only in 2 patients. Data for patient 1 have been previously reported.8 In patient 9, who presented with right lateral WPW-type VP, transesophageal study revealed a preexcited RR interval of 240 ms; the patient refused catheter ablation and died 3 years after the last examination. None of the patients had an ECG tracing at the time of cardiac arrest.
Pathological Data
Gross Examination
Heart weight (360±90 g) and left ventricular
(12.5±1.0 mm), right ventricular (4±0.5 mm), and interventricular
septal (12.5±1.5 mm) thicknesses were normal. Origin and course of the
coronary arteries were regular in the absence of obstructive coronary
artery disease. AV and semilunar valves were normal in all but patient
6, who presented with mitral valve prolapse. Patient 9 had previous
surgical closure of patent ductus arteriosus.
Ordinary Myocardium Histology
No patient exhibited inflammatory infiltrates, myocytes
necrosis or disarray, interstitial or replacement-type fibrosis, or
fatty infiltration of the ventricular myocardium. Intramural small
vessels were normal.
Focal, active myocarditis, which consisted of patchy
inflammatory infiltrate with myocyte necrosis, occurred in 4 (50%)
patients with WPW-type VP and was confined to the atrial myocardium.
Inflammatory cell foci were multiple and bilateral and involved the
myocardium around the pulmonary vein orifices in 2 cases, either close
to (n=2) or far away from (n=2) the atrial ending of the accessory
fascicle, but never did these foci affect the fascicle or conducting
tissue (sinus node and AV junction). According to immunohistochemical
findings, the inflammatory infiltrate was polymorphous in 1
(Figure 1) and lymphocytic (mostly activated T-lymphocytes,
CD43 and CD45RO positive)
(Figure 2) in 3 cases.
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Control hearts did not show macroscopic or histological abnormalities; in particular, evidence of atrial myocarditis was never found.
Conduction System Investigation
LGL Syndrome
The sinus node structure was normal in both cases.
Congenital AV nodal hypoplasia in patient
18 and right-sided
atrio-Hisian tract in patient 2 were found. The latter was in a
conspicuous atrial fascicle of ordinary and transitional myocardium and
bypassed a morphologically normal AV node to anastomose distally with
the common His bundle (the so-called James or Paladino
fascicle).
WPW Syndrome
Sinus and AV nodal in addition to common His bundle and
bundle branch anatomy was normal in all cases but 1 (patient 3), in
whom the left bundle branch divided early in 2 parts, 1 subendocardial
and 1 intramural septal, whereas the proximal right bundle branch
insulated a cluster of ordinary myocytes to delineate a circuit. By
serial histological sectional study of the septal and lateral AV
junctions, 10 accessory AV pathways were found, which were located as
expected by -wave morphology on surface ECG in the left lateral ring
in 7
(Figure 1
) (double accessory pathways in patient 5) and right
posterolateral ring in 2
(Figure 2); 1 of the latter was associated with a septal
accessory AV pathway because of a gap in the fibrous septal annulus,
which accounts for a mild Ebstein
anomaly.9 (See
Table 2.)
These accessory AV pathways were all composed of ordinary myocardium,
which accounts for the continuity between atria and ventricles. In the
2 hearts with right-sided connections, the accessory bundle typically
crossed the AV groove at the point at which the fibrous annulus showed
a gap. In contrast, left-sided AV connections always occurred in the
presence of a well-formed fibrous annulus. Lateral AV accessory
pathways showed a mean thickness of 310±190 µm, a mean distance from
the endocardium of 750±530 µm, and a mean distance from the
epicardium of 7610±1420 µm. Moreover, left lateral AV accessory
pathways had a mean distance from the coronary sinus of 4430±1570
µm. (See
Table 2.)
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By comparing left-sided and right-sided accessory pathways, we found a significantly greater distance only from the epicardium of the former (8028±1290 versus 6160±791 µm; P=0.04). No difference was observed as far as thickness (247±52 versus 530±170 µm; P=NS) and distance from the endocardium (814±582 versus 530±325 µm; P=NS).
Curiously, the lateral bypass tract showed a vertical course
in 5 cases (all left sided), whereas this tract presented an irregular
and sinuous horizontal course in the remaining 4 cases (2 left-sided
and 2 right-sided accessory AV pathways). In the patient with
intermittent VP (patient 10), the myocardium of the accessory pathway
was partially replaced by fibrous tissue at the ventricular end, at
which only scattered residual muscular fibers were visible
(Figure 1).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Present Study
A 3.6% prevalence of VP in our series of young SD victims has been found. The fatal event was not preceded by warning symptoms in 40% of patients, and death almost invariably occurred at rest, often during sleep. Thus, occurrence of death was relatively unpredictable. As far as morphological findings, a left accessory pathway was the most frequent substrate; it consisted of a very thin muscular structure with a mean thickness of 310 µm located close to the endocardium. Surprisingly enough, ordinary myocardium histology revealed isolated acute atrial myocarditis in 50% of the patients, which was never detected in any control heart.
VP and SD in Young People
Estimated prevalence of WPW VP is 0.1 to 3.1 cases per
100010 11 12
and the overall risk of SD is low, reportedly occurring at a rate of
0.6% per
year.1 2 3
No systematic data are available on prevalence of VP among SDs in the
young,13 14 15 16
and our figures are probably underestimated, given that the conditio
sine qua non for diagnosis was the availability of ECG tracing, a
criterion fulfilled in only one third of cases. Notably, the 6% of SDs
that remained unexplained after postmortem examination were in patients
for whom no ECG tracing was done, which thus raises the suspicion of
either hidden conduction-system abnormalities or nonstructural
diseases. Likewise, by obtaining an ECG in nearly 50% of 57 apparently
normal hearts referred for investigation of SD,
Davies17 was able to
diagnose VP in 7, in which subsequent study revealed accessory AV
pathways.
Anatomic Substrates of VP
Accessory AV connections predisposing to VP may be
"direct," which are connections located outside the specialized AV
junction that directly connect the atrial and ventricular myocardium
(Kent fascicle) or "mediated," which involve the specialized AV
junction and either connect the septal atrial myocardium with the His
bundle (James or Brechenmacher fibers) or the Tawarian system with the
ventricular myocardium (Mahaim
fibers).18 19
A rare condition that promotes early ventricular excitation is the so-called enhanced AV conduction or LGL syndrome.20 21 The impulse runs very quickly through the His bundle, with a short PR interval and a normal QRS complex. Two histological backgrounds in our series explained the missed delay at the AV node level. One is a congenitally hypoplastic AV node, which created a lessened bulk of specialized tissue to delay impulse transmission from atria to ventricles.8 The second is presence of an atrio-Hisian bundle that bypasses the AV node and transmits the activation signal directly to the His bundle.22 23 In both substrates, the onset of atrial fibrillation may precipitate ventricular fibrillation as it occurs in the WPW syndrome.
In WPW syndrome, an aberrant myocardial fascicle joins the atria to the ventricles beyond the specialized AV junction.23 24 25 26 This fascicle usually is located in the lateral rings and consists of a thin muscular segment that does not possess decremental conduction properties7 and may serve not only as bypass tract for VP but also as a limb for an AV reentry circuit, which accounts for a reciprocating supraventricular tachycardia. Impedance mismatch between the tiny anomalous fibers and the ventricular muscle bulk in addition to partial replacement of the accessory fascicle by fibrous tissue, as in 1 of our cases, might explain intermittent impaired antegrade conduction.27 Moreover, the accessory fascicle along the AV sulcus was always located close to the endocardium; size and site are such that Kent’s bundle is easily amenable to endocardial transcatheter ablation, the current procedure to reestablish AV electrical connection through the His bundle.28
Different sets of criteria for the localization of accessory pathways have been proposed on the basis of polarity of the QRS complex on various ECG leads. The present study confirms that the 12-lead ECG can be a good indicator of the site of accessory AV connection when the criteria of Arruda et al are applied.6
Pathophysiology of SD in VP
Cardiac arrest is believed to be related to the
occurrence of atrial
fibrillation,2 which may
convert into ventricular fibrillation if the refractory period of the
accessory pathway is short. The clinical profile of patients with WPW
syndrome at risk of SD comes from the examination of those resuscitated
from ventricular fibrillation. When compared with WPW patients without,
those with ventricular fibrillation show a higher prevalence of both AV
reentrant tachycardia and atrial fibrillation and are more likely to
have multiple accessory AV
pathways.29 Moreover, the
shortest RR interval between the preexcited beats is <250 ms, as a
result of rapid ventricular response over the accessory pathway. This
feature, which was present in the only patient who underwent
transesophageal study in our series, is considered the most important
risk factor for the development of ventricular fibrillation. A patient
with Ebstein’s anomaly or other concomitant heart disease is probably
also at greater risk for ventricular fibrillation. Although patients
with ventricular fibrillation or atrial fibrillation no doubt merit
full electrophysiological investigation and interventional therapy,
considerable controversy still exists regarding the need for
prophylactic treatment in asymptomatic individuals in whom the disease
has been diagnosed by
chance.30 However, these
subjects have a small but definite risk of experiencing cardiac arrest
as first manifestation of the disease, given that it occurred in half
of our cases.
Isolated Atrial Myocarditis as a Substrate of
Paroxysmal Atrial Fibrillation
Atrial fibrillation is reported in 20% to 30% of
patients with WPW syndrome31
and may be accounted for by primary atrial pathology or be secondary to
AV reentrant tachycardia. Typically, the electrophysiologic mechanism
of atrial fibrillation consists of multiple migratory reentrant wave
fronts of activation in both atria. This represents the rationale for
curative therapy by surgical atriotomies or catheter-mediated ablation
lines.32 Recently it has
been suggested that, in a subset of young patients without structural
heart disease, atrial fibrillation may be initiated by a focal rapidly
firing source of activity.33
In this setting, abnormal automaticity or triggered activity is the
most likely mechanism. The anatomic substrate of electrical atrial
instability is difficult to investigate in vivo, because it requires
either a surgical or, even rarer, an atrial biopsy approach. In the
present fatal WPW cases, a 50% incidence of isolated atrial
myocarditis was found. This finding, despite the absence of a final ECG
tracing, supports the hypothesis that atrial inflammatory foci may act
as a trigger of paroxysmal atrial fibrillation, which in turn
precipitates SD due to very rapid ventricular conduction. Recent data
suggest that lone paroxysmal atrial fibrillation may be due to isolated
atrial myocarditis. In a series of 12 patients with drug-refractory
paroxysmal atrial fibrillation studied by atrial endomyocardial biopsy,
Frustaci et al34 found
isolated atrial lymphocytic myocarditis in 66% of cases. The
cause-effect relationship between myocarditis and atrial fibrillation
was further supported by the absence of atrial fibrillation recurrence
in patients treated with steroids during a mean follow-up of 12 months.
More recently, Maixent et
al35 demonstrated the
presence of circulating autoantibodies against myosin heavy chain in
60% of patients with idiopathic paroxysmal atrial fibrillation, which
raises the possibility of an autoimmune process. Moreover,
Rossi36 looked at a small
series of patients with atrial flutter or fibrillation and found
striking right atrial inflammatory changes in 5 of 8 cases. Notably,
the possibility of an isolated arrhythmogenic atrial myocarditis was
put forward by Fromer et
al,37 who studied 2 cases
with drug-refractory ectopic atrial tachycardia; surgically resected
atrial tissue showed focal myocarditis in the absence of concomitant
ventricular abnormalities at endomyocardial biopsy associated with a
minor elevation of antibodies against echovirus in 1 case. However, due
to the intrinsic limitations of a postmortem study of formalin-fixed
specimens and the inherent lack of feasibility of molecular biology
investigation, the cause of the atrial inflammation remains
intriguing.
In summary, 40% of young SD victims with VP experienced cardiac arrest as the first manifestation of the disease. In such patients, isolated atrial myocarditis may act as a trigger of paroxysmal atrial fibrillation leading to SD. This may account for the unpredictability of atrial fibrillation onset and difficulty on risk stratification.
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Acknowledgments |
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This study was supported by Veneto Region, Venice, Italy and Murst, Rome, Italy. We thank Alessandra Dubrovich, Agostino Leorin, Mauro Pagetta, and Anna Saracino for the excellent technical support and Chiara Carturan for editorial assistance. The support of Fondazione Cassa di Risparmio di Padova e Rovigo is also acknowledged.
Received June 21, 2000; revision received August 7, 2000; accepted August 18, 2000.
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M. Pieroni, C. Chimenti, A. Frustaci, K. Nanthakumar, Y. R. Lau, V. J. Plumb, A. E. Epstein, and G. N. Kay Letter Regarding Article by Nanthakumar et al, "Electrophysiological Findings in Adolescents With Atrial Fibrillation Who Have Structurally Normal Hearts" * Response Circulation, January 25, 2005; 111(3): e27 - e27. [Full Text] [PDF]
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M. Arad, I. P. Moskowitz, V. V. Patel, F. Ahmad, A. R. Perez-Atayde, D. B. Sawyer, M. Walter, G. H. Li, P. G. Burgon, C. T. Maguire, et al. Transgenic Mice Overexpressing Mutant PRKAG2 Define the Cause of Wolff-Parkinson-White Syndrome in Glycogen Storage Cardiomyopathy Circulation, June 10, 2003; 107(22): 2850 - 2856. [Abstract] [Full Text] [PDF]
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M. H. Gollob, J. J. Seger, T. N. Gollob, T. Tapscott, O. Gonzales, L. Bachinski, and R. Roberts Novel PRKAG2 Mutation Responsible for the Genetic Syndrome of Ventricular Preexcitation and Conduction System Disease With Childhood Onset and Absence of Cardiac Hypertrophy Circulation, December 18, 2001; 104(25): 3030 - 3033. [Abstract] [Full Text] [PDF]
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