Stefan Peters* Introduction. Methods. * Corresponding author. Tel: þ address:
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1 Europace (2008) 10, doi: /europace/eun030 Arrhythmogenic right ventricular dysplasia-cardiomyopathy and provocable coved-type ST-segment elevation in right precordial leads: clues from long-term follow-up Stefan Peters* Klinikum Quedlinburg, Department of Cardiology, Academic Teaching Hospital of the University Hospital Magdeburg, Ditfurter Weg 24, Quedlinburg, Germany Received 29 October 2007; accepted after revision 19 January 2008; online publish-ahead-of-print 27 February 2008 KEYWORDS Brugada phenomenon; Arrhythmogenic right ventricular cardiomyopathy; Ajmaline challenge; Conduction disease; Molecular genetics Introduction Since the first description of typical Brugada-type ECG, overlap with arrhythmogenic right ventricular cardiomyopathy (ARVC) has been discussed. 1 4 According to molecular findings in the SCN5A gene, Brugada syndrome has been classified as pure repolarization abnormality. 5 Recently, data were published that Brugada syndrome can be caused by depolarization abnormalities 6 and is associated with myocardial fibrosis due to molecular genetic background in individual cases. 7 * Corresponding author. Tel: þ address: s.peters@klinikum-quedlinburg.de Aims Provocable coved-type ST-segment elevation in right precordial leads is an observation in 16% of patients with typical arrhythmogenic right ventricular cardiomyopathy (ARVC). The value of this observation should be analysed in a long-term follow-up of 17 patients identified by systematic ajmaline Methods and results At first evaluation, one female had an aborted sudden cardiac death and eight patients suffered from recurrent syncopes. Intrathoracic cardioverter defibrillator (ICD) implantation was done in the patient with aborted sudden cardiac death and in six patients with recurrent syncopes. One of these six patients had intermittant 2 38 AV block. Another patient had inducible ventricular tachycardia (VT) at electrophysiological study. Follow-up over more than 3 years in all but one patient was characterized by documented monomorphic VT in the patient with inducible VT and ICD implantation (6%). The patient with aborted sudden cardiac death had only non-sustained VT s shortly after ICD implantation. From the eight patients without syncopes two more patients developed AV block and SA block 38 (18%). Lead-associated complications appeared in three of eight patients with ICDs (38%). Repeated ajmaline challenge was positive in four of eight cases (50%). One patient had a new mutation encoding for SCN5A gene. Conclusion Ajmaline challenge in typical ARVC characterizes a subgroup of elderly, predominantly female patients with the risk of developing conduction disease. Tachycardia-related events are rare. The indication of ICD implantation in recurrent syncopes is critical as the rate of lead-associated complications in a more than 3 years follow-up is high. In a previous study, we showed that systematic ajmaline challenge in patients with typical ARVC could provoke coved-type ST elevation in right precordial leads in 16%. 8 The value of provocable coved-type ST elevation in ARVC should be analysed by a long-term follow-up of 17 patients who could be identified by systematic ajmaline challenge performed in 106 patients with traditional 9 and modified 10 ISFC/ESC criteria of ARVC. Methods Ajmaline challenge was performed as a bedside test by administration of 1 mg/kg body weight intravenuously over 3 5 min under continuous monitoring of precordial leads at standard position without temporary pacemaker insertion but with defibrillator in Published on behalf of the European Society of Cardiology. All rights reserved. & The Author For permissions please journals.permissions@oxfordjournals.org.
2 Arrhythmogenic right ventricular dysplasia-cardiomyopathy and provocable coved-type ST-segment elevation 817 stand-by after written informed consent in 106 unrelated patients with the diagnosis of ARVC according to traditional and modified ISFC/ESC criteria by right ventricular angiography, transthoracic echocardiography, exercise testing, Holter monitoring, standard and highly amplified (20 mv) and modified ECG (bipolar leads in position V2, V3, and V5), and family history. According to traditional diagnostic criteria, 43 patients had two major and 63 patients had one major and two minor diagnostic criteria. Family history of ARVC was evident in 20 patients by systematic family screening and in additional 43 patients by family history. Clinical, electrocardiographic, electrophysiological characteristics, and right ventricular morphological findings of all 106 patients with positive (n ¼ 17) and negative ajmaline challenge (n ¼ 89) are summarized in Table 1. A positive ajmaline challenge was defined as coved-type ST-segment elevation in at least one right precordial lead of at least 2 mm. Conduction disease (see Table 1) was defined as intermittent 2 or 38 atrioventricular or sinuatrial block. Programmed ventricular stimulation was done from the right ventricular apex and the right ventricular outflow tract with up to three extra stimuli with a minimal coupling interval of 180 ms or after reaching refractoriness at a basic cycle length of 500, 400, and 330 ms. All but one patient with positive ajmaline response had a minimum follow-up of 3 years (mean follow-up of years) with repeated ajmaline testing in eight cases and repeated electrophysiological study because of recurrence of symptoms in two cases. Seven patients with initial intrathoracic cardioverter defibrillator (ICD) implantation due to recurrent syncopes in six cases and aborted sudden cardiac death in one case had ICD controls in a regular time interval of 6 months. Follow-up data from ajmaline-positive patients were analysed with regard to spontaneous major arrhythmic events (arrhythmic death, ventricular tachycardia (VT), aborted sudden cardiac death and bradycardia due to sinuatrial or atrioventricular block) and arrhythmic events in the Holter of the implanted ICDs. In 17 patients with positive ajmaline response molecular genetics was done at the University Hospital of Muenster, Germany (Prof. Dr E. Schulze-Bahr) with analysis of mutations encoding for the plakophilin-2 gene and the SCN5A gene as a research project with special funding. Results Patient characteristics In 17 patients (3 males, 14 females, mean age years) ajmaline challenge could provoke coved-type right Table 1 precordial ST elevation. These patients were older, were more commonly of female gender and reported syncope more often than 89 patients with negative ajmaline test (59 males, 30 females, mean age years) as shown in Table 1. Both groups were comparable in terms of electrocardiographic and echocardographic parameters (see Table 1). Figure 1 shows typical electrocardiographic ARVC findings before and typical Brugada phenomenon after ajmaline Electrophysiological study results Electrophysiological studies were performed in 13 patients with provocable Brugada phenomenon (76%) and in only 16 cases (18%) with negative ajmaline response. Data of EP study results are included in Table 1. His ventricle (HV) intervals were normal in all patients examined. Repeated EP studies for recurrent symptoms were done in two patients with Brugada phenomenon again without inducibility of ventricular arrhythmias. Repeated ajmaline challenge In four from eight patients, repeated ajmaline challenge turned to be negative. In the other four patients, ajmaline challenge was again positive. Standard ECG and highly amplified and modified ECG findings were completely identical in all eight patients in comparison to the first evaluation. Right ventricular abnormalities could be repeatedly confirmed by transthoracic echocardiography. Molecular genetics A polymorphism of the plakophilin-2 gene, which was also detectable in more than 2% of a normal population, could be found in one patient. In all patients already known mutations encoding for plakophilin-2 could be excluded. A heterocygote, up to now unpublished mutation in the SCN5A gene (2236 G.A, E746K) could be found in one patient. Polymorphism could be ruled out by exclusion of this mutation in a normal population. This patient had in addition to diagnostic steps at the initial evaluation cardiac MRI with fatty infiltration of the right ventricular Clinical, electrocardiographic, electrophysiological, and morphological findings in the whole group of 106 patients with ARVC Characteristics Positive ajmaline (n ¼ 17) Negative ajmaline (n ¼ 89) P Age, mean (years) ,0.025 Male female 1:5 2:1,0.001 Syncopes n ¼ 8 (47%) n ¼ 15 (17%),0.01 Aborted SCD n ¼ 1 (6%) n ¼ 6 (7%) 0.85 Spontaneous VT n ¼ 0 n ¼ 28 (31%),0.025 r.prec.qrs prolongation n ¼ 17 (100%) n ¼ 89 (100%) 1 r.prec. T-inv..V1 n ¼ 9 (53%) n ¼ 49 (55%) 0.75 r.prec. epsilon waves n ¼ 13 (76%) n ¼ 67 (75%) 0.89 EP study done n ¼ 13 (76%) n ¼ 16 (18%), Inducible VT/VF n ¼ 1 (6%) n ¼ 2 (12.5%) 0.55 Conduction disease n ¼ 1 (6%) n ¼ 1 (1%) 0.2 Major RV abn. n ¼ 6 (35%) n ¼ 37 (42%) 0.15 Minor RV abn. n ¼ 11 (65%) n ¼ 52 (58%) 0.15 SCD, sudden cardiac death; VT, ventricular tachycardia; r.prec., right precordial; T-inv., T wave inversions; EP, electrophysiological; VF, ventricular fibrillation; RV, right ventricular; abn., abnormalities.
3 818 S. Peters Figure 1 Precordial leads of a patient with typical ARVC findings before and with typical Brugada phenomenon after ajmaline Figure 2 Precordial leads before and after ajmaline administration in the patient with SCN5A mutation. free wall and segmental hypokinesia of the apex and the inferior, subtricuspid area. Figures 2 4 show precordial ECG leads before and after ajmaline challenge, right ventricular angiogram at 308 RAO projection and MRI scan of this patient. Follow-up Patients with provocable Brugada phenomenon had a low risk of ventricular tachyarrhythmias with monomorphic VT in only one patient (6%). Figure 3 Right ventricular angiography in 308 RAO projection of the patient with SCN5A mutation. Figure 4 In addition to one patient with AV block at the initial evaluation, two more female patients developed 38 atrioventricular block and 38 sinuatrial block in the follow-up after 2 and 3 years, respectively (18%). One patient received an ICD and the other 79-year-old patient received a pacemaker implantation without further arrhythmic events. Three from eight patients (38%) had lead-associated complications of the ICD with necessary re-intervention after 1, 2, and 3 years, respectively. Discussion MRI scan of the patient with SCN5A mutation. The value of systematic ajmaline challenge in cases with ARVC whose results were first published in is up to now completely uncertain. Data of long-term follow-up presented in this paper reveal that positive coved-type ST segment elevation in right precordial leads in ARVC differentiate a subgroup of elderly, predominantly female patients with progressive conduction disease whereas the risk of ventricular tachyarrhythmias is
4 Arrhythmogenic right ventricular dysplasia-cardiomyopathy and provocable coved-type ST-segment elevation 819 low. If patients with ARVC, provocable Brugada phenomenon and recurrent syncopes are treated by ICD implantation lead-associated complication rate is much higher than the rate of ventricular tachyarrhythmias. Similar findings have been described in a French cohort of Brugada syndrome. 11 From this point of view, the results of the ajmaline test cannot be used in order to select patients for ICD implantation. It seems that with regard to the risk of ventricular tachyarrhythmias the provocation of ST elevation by ajmaline in patients with ARVC represents a false positive result. The discussion remains whether a mean follow-up of 4 years is enough to answer this question. In the first systematic pathological workup of a small number of patients with ARVC, 12 the specialized conduction system was spared. Whether this is really the fact in most cases of ARVC is questionable as a French working group with the up to now largest number of patients with ARVC at autopsy could demonstrate a high percentage of fatty, fibrous or fibrofatty abnormalities of the conduction system. 13 The long-term follow-up findings of the present paper seem to confirm these data within a subgroup of patients identified by ajmaline Although the use of ajmaline for demasking conduction abnormalities is not new 14,15 the occurrence of right precordial coved-type ST elevation as the typical finding of Brugada syndrome 16,17 was not yet described in this setting. Another interesting point is that repeated ajmaline challenge was positive in only 50% of patients. This leads to the discussion whether myocarditis of the right ventricle in ARVC is the reason for initial positive ajmaline challenge with negative results after healing of myocarditis. A similar observation has been described in Chagas disease where ajmaline was used a couple of years ago for demasking acute myocarditis. 18 A high amount of myocarditic changes in the myocardium of patients with Brugada syndrome could be demonstrated by Frustaci et al. 19 Basically, the question remains whether the patients followed in this series represent a typical form of ARVC as endomyocardial biopsies were not taken. Nevertheless, the diagnosis of ARVC can be supposed in all cases by traditional and modified ISFC/ESC diagnostic criteria. Electrocardiographic findings and right ventricular morphology was comparable in patients with and without ajmaline response. Owing to a low number of EP studies in the ajmaline-negative group because of asymptomatic affected in systematic family screening and ICD implantation without EP study in cases with spontaneous VT the rate of inducible VT at EP study in both groups was nearly identical. The only difference between these two groups was the much higher presence of syncopes in the ajmaline-positive group and the higher occurrence of spontaneous VT s in the ajmalinenegative group. ARVC cases in a non-referral centre are in general characterized by lower numbers of life-threatening ventricular arrhythmias and higher rate of syncopes not always explained by ventricular tachyarrhythmias. 20 With regard to molecular genetics the exclusion of mutations encoding for the plakophilin-2 gene as the major cause of familial forms of ARVC in the ajmalinepositive subgroup is of importance. It appears to be likely that an up to now not reported genetic background exists for the association of ARVC and Brugada phenomenon. Also of interest is the finding of an up to now not published mutation encoding for the SCN5A gene in one of the patients in this group. Whether this mutation has caused structural abnormalities is highly speculative. However, in individual cases SCN5A mutations can produce significant myocardial fibrosis. 7 Limitations of the study As molecular genetics was only possible as a part of a research project with special funding only mutations encoding for plakophilin-2 and SCN5A could be investigated in the patients. Conflict of interest: none declared. References 1. Martini B, Nava A, Thiene G, Buja GF, Canciani B, Scognamiglio R et al. Ventricular fibrillation without apparent heart disease: description of six cases. Am Heart J 1989;118: Tada H, Aihara N, Ohe T, Yutani C, Hamada S, Miyanuma H et al. Arrhythmogenic right ventricular cardiomyopathy underlies syndrome of right bundle branch block, ST-segment elevation and sudden death. Am J Cardiol 1998;81: Izumi T, Ajiki K, Nozaki A, Takahashi S, Tabei F, Hayakawa H et al. Right ventricular cardiomyopathy showing right bundle branch block and right precordial ST segment elevation. Intern Med 2000;39: Corrado D, Basso C, Buja G, Nava A, Rossi L, Thiene G. Right bundle branch block, right precordial ST-segment elevation, and sudden death in young people. Circulation 2001;103: Antzelevitch C. Role of spatial dispersion of repolarization in inherited and acquires sudden cardiac death syndromes. Am J Physiol Heart Circ Physiol 2007;293:H Tukkie R, Sogaard P, Vleugels J, de Groot IK, Wilde AA, Tan HL. Delay in right ventricular activation contributes to Brugada syndrome. Circulation 2004;109: Coronel R, Casini S, Koopmann TT, Wilms-Schopman FJ, Verkerk AO, de Groot JR et al. Right ventricular fibrosis and conduction delay in a patient with clinical signs of Brugada syndrome: a combined electrophysiological, genetic, histopathologic, and computational study. Circulation 2005;112: Peters S, Trümmel M, Denecke S, Koehler B. Results of ajmaline testing in patients with arrhythmogenic right ventricular dysplasiacardiomyopathy. Int J Cardiol 2004;95: McKenna WJ, Thiene G, Nava A, Fontaliran F, Blomstrom-Lundqvist C, Fontaine G et al. Task force of the working group myocardial and pericardial disease and the European Society of Cardiology and the Scientific Council on Cardiomyopathies of the International Society and Federation of Cardiology. Diagnosis of arrhythmogenic right ventricular dysplasia/ cardiomyopathy. Br Heart J 1994;71: Peters S. Advances in the diagnostic management of arrhythmogenic right ventricular dysplasia-cardiomyopathy. Int J Cardiol 2006;113: Sacher F, Probst V, Iesaka Y, Jacon P, Laborderie J, Mizon-Gerard F et al. Outcome after implantation of a cardioverter-defibrillator in patients with Brugada syndrome: a multicenter study. Circulation 2006;114: 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: Tabib A, Loire R, Chalabreysse L, Meyronnet D, Miras A, Malicier D et al. Cicumstances of death and gross and microscopic observations in a series of 200 cases of sudden death associated with arrhythmogenic right ventricular cardiomyopathy and/or dysplasia. Circulation 2003;108: Gronda M, Rognoni G, D Aulerio M, Occhetta E, Rossi P. Prognostic evaluation of infranodal conduction abnormalities by ajmaline and overdriving test (author s transl). G Ital Cardiol 1980;10: David D, Cabanis C, Guize L, Le Heuzey JY, Carcone P, Née Met al. Clinical and electrophysiological aspects of median intra-his bundle block with normal electrocardiogram at rest. Arch Ma Coeur Vaiss 1985;78: Rolf S, Bruns HJ, Wichter T, Kirchhof P, Ribbing M, Wasmer K et al. The ajmaline challenge in Brugada syndrome: diagnostiv impact, safety, and recommended protocol. Eur Heart J 2003;24: Hong K, Brugada J, Oliva A, Berruezo-Sanchez A, Potenza D, Pollevick GD et al. Value of electrocardiographic parameters and ajmaline test in the
5 820 S. Peters diagnosis of Brugada sindrome caused by SCN5A mutations. Circulation 2004;110: Chiale PA, Przybylski J, Laino RA, Halpern MS, Sanchez RA, Gabrieli A et al. Electrocardiographic changes evoked by ajmaline in chronic chagas disease without manifest myocarditis. Am J Cardiol 1982;49: Frustaci A, Priori SG, Pieroni M, Chimenti C, Napolitano C, Rivolta I et al. Cardiac histological substrate in patients with clinical phenotype of Brugada syndrome. Circulation 2005;112: Peters S, Trümmel M, Meyners W. Prevalence of right ventricular dysplasia-cardiomyopathy in a non-referral hospital. Int J Cardiol 2004; 97:
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