Do You Have to Continue Taking Tikosyn if You Have an Av Node Ablation
Abstract
Treatment strategy for atrial fibrillation (AF) is a controversial matter. Catheter ablation is increasingly being used to treat patients with AF, and recent studies have reported success rates >80% for paroxysmal AF and >70% for persistent AF. The purpose of this work is to review the evidence supporting catheter ablation and compare it with pharmacological treatment in the management of AF.
Atrial fibrillation (AF) is the most prevalent cardiac arrhythmia yet the ideal treatment strategy is hotly debated. Large randomized trials have failed to demonstrate a mortality benefit of a pharmacologically based rhythm control strategy compared with a rate-controlled strategy, even in patients with left ventricular dysfunction. 1–4 This has led to a widespread belief that restoration of sinus rhythm by any means is unnecessary, despite the known increase in morbidity and age-matched mortality risk. 5 However, we believe that restoration of sinus rhythm is a desirable aim. In an era where AF ablation is becoming standard practice in centres across the world, it is justified to revisit the evidence for its application and the role pharmacological treatment of AF still holds.
Comparing ablation and anti-arrhythmic drug
Several difficulties arise when trying to compare drugs and ablation trials, as major differences in design and endpoint definition exist. Success can, therefore, be defined by the absence of arrhythmia recurrence during follow-up, or reduction in arrhythmia burden, or sinus rhythm at last follow-up, or the endpoint can be the time to first arrhythmia recurrence. These disparities challenge the possibility to compare the efficiency of each intervention, and few studies have made direct comparisons between anti-arrhythmic drug (AAD) and ablative treatment for AF.
It is also a difficult task to compare ablation trials among themselves, as there is no standard approach for AF ablation and different centres use different strategies and techniques. Moreover, there is not yet a standardized way to report outcome. The use of AAD is also variable from study to study. These pitfalls should be kept in mind while reviewing the data presented.
Sinus rhythm: a worthy quest?
Atrial fibrillation is associated with an excess in mortality and higher morbidity, with, among other factors, up to five-fold increased risk of stroke compared with an age-matched AF-free population when co-morbidities have been adjusted for. 6–10 However, when large randomized controlled trials tried to demonstrate a benefit of sinus rhythm by pharmacological means, the results were perhaps surprising. The PIAF study was the first to suggest that a pharmacological rate control strategy was comparable with a rhythm control strategy achieved by drugs and/or DC cardioversion. 4 The RACE and AFFIRM studies further supported these findings by suggesting that both strategies were equivalent in terms of mortality and adverse event rates including strokes, and recently, this statement could be extended to patients with heart failure following the publication of the AF CHF trial. 1–3 This led to a widespread belief that rhythm control was the strategy of choice for patients with AF. However, what these studies did not take into account was the effect of the AADs themselves.
When the AFFIRM trial data were re-analysed using an on-treatment analysis method, it was found that sinus rhythm was associated with a 47% increase in survival compared with AF (HR 0.53) and that the use of AADs increased mortality by 49% (HR 1.49). 5 Similarly, sinus rhythm conferred a better prognosis both for patients treated with dofetilide and patients taking placebo, with a 56% reduction in mortality compared with patients in AF (HR 0.43and 0.38, respectively). 11 Therefore, although evidence suggested an advantage of sinus rhythm over AF, this beneficial effect seemed to be mitigated by the adverse effects of the drugs used to achieve and maintain it. Catheter ablation can now restore sinus rhythm and obviate the need for long-term AAD therapy in the majority of patients. Whether a survival advantage can be achieved by restoring sinus rhythm with ablation is an attractive possibility that is still unanswered.
Methods
A systematic review of the literature using the Pubmed database was conducted using the terms AAD, AF, surgery, catheter ablation, and atrial arrhythmia. Eight studies and two review articles were found comparing AAD and catheter ablation for AF. Randomized controlled studies on AAD, catheter ablation, and surgical trials for AF were also reviewed.
Rhythm control
Anti-arrhythmic drugs
AADs have scored rather poorly in maintaining sinus rhythm over time. In comparative studies, amiodarone consistently stands out as the most efficient drug to prevent atrial arrhythmia recurrences. However, even in trials where amiodarone achieved the highest rate of SR, recurrences occurred in 35%. 12 Class 1C AADs were shown to suppress AF recurrences in 30 to 63% in patients with repetitive episodes of AF, whereas sotalol efficiently maintained SR in 32–73%. 13–16 Newer drugs such as dofetilide successfully maintained SR at 1 year in 79% of patients with AF and concomitant heart failure, compared with 42% in the placebo group. 11 Recently, dronedarone was shown to delay the time to the first AF recurrence from 53 days in the placebo group to 116 days in the treatment group. At 1 year, AF had recurred in 64.1% of patients taking dronedarone compared with 72.5% taking placebo. 17
In trials comparing rate vs. rhythm control strategies using multiple AADs, the rate of sinus rhythm maintenance in the rhythm control groups ranged from 39% after a mean of 2.3 years in RACE, 3 56% at 1 year, 4 to up to 82.4% at 1 year, and 62.6% at 5 years in AFFIRM, considering 34.6% in the rate control group were also in sinus rhythm at 5 years. 1 In the AF-CHF study, 73% of patients assigned to rhythm control were in sinus rhythm after a mean follow-up of 3 years compared with <30% in the rate control group. However, 58% in rhythm control had experienced at least one recurrence of AF during the follow-up period 2 (Table1). These results must be interpreted taking into consideration that in this latter trial, a significant proportion of patients had paroxysmal AF (33%). In the other trials, a significant number of patients had persistent AF, and inclusion in the study often occurred after cardioversion to SR.
Table 1
Anti-arrhythmic drugs and maintenance of sinus rhythm
AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm.
Table 1
Anti-arrhythmic drugs and maintenance of sinus rhythm
AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm.
Drugs, therefore, have been shown to have limited efficacy in controlling rhythm. Moreover, the outcome (the rate of patients in sinus rhythm at last follow-up) was not a true reflection of rhythm control, nor of AF burden, because episodes of AF occurring between visits were not considered, and efficacy is, therefore, overestimated.
Atrial fibrillation ablation: rationale
Ablation strategies have evolved rapidly over the past years. Initial surgical techniques aiming at treating AF were based on the hypothesis that the fibrillatory process was generated by multiple wavelets propagating through the atria, 18,19 and that compartmentalization of the atria would interrupt re-entry circuits maintaining the fibrillation and, therefore, render the heart incapable of sustaining AF. 20,21 The finding that AF was triggered in most patients by ectopic activity arising from the pulmonary veins (PVs) then shifted interest towards abolishing these triggers 22 (Figure1). In persistent AF however, AF is not dependent solely on PV triggers and becomes self-sustained by sources and re-entry zones located outside the veins, as atrial remodelling is promoted by the continuing arrhythmia and leads to the atrium's ability to sustain further fibrillation, giving rise to the concept that 'AF begets AF'. 23
Figure 1
Example of a case: 65-year-old male with paroxysmal atrial fibrillation. The patient arrived in atrial fibrillation, sinus rhythm was restored by isolation of the right superior pulmonary vein, and fibrillation was still seen inside the vein after isolation. This demonstrates the arrhythmogenicity of the pulmonary veins and suggests that the right superior pulmonary vein was a significant atrial fibrillation trigger for this specific patient. (A) Isolation of the right superior pulmonary vein restores sinus rhythm. (B) Ongoing atrial fibrillation inside the isolated right upper pulmonary vein despite atrial sinus rhythm. (C) Position of the circular mapping catheter inside the right superior pulmonary vein, quadripolar inside the coronary sinus, and RF catheter at the lower part of the ostium of the right superior pulmonary vein, where isolation was obtained.
Surgical approach to atrial fibrillation
The maze procedure modified to become the Cox maze III procedure consist in creating a series of incisions in both atria to prevent the formation of macro-re-entrant circuits implicated in the maintenance of AF. 24 These lesions sets have proved to successfully eliminate AF in up to 97% of patients, among whom 76% did not need AADs at 5 years of follow-up (Figure2). 25 However, the need for an open-heart surgery along with inherent risks and subsequent convalescence restricted the use of this technique mainly to patients undergoing concomitant heart surgery for other purposes or to patients with contraindications to other treatments for AF. The development of minimally invasive techniques (MISAA, minimally invasive surgical AF ablation) through minithoracotomy where ganglionic plexi, PV antrum, and Marshall vein are ablated and LAA is excised has widened the indication for surgical management of AF. The complication rate of MISAA is reported around 8%, whereas it reaches 19% for the Cox maze III, and the success rates at 1 year from 65 to 91% without AADs. 26–28 Patients who may benefit from MISAA include patients with failure to catheter ablation and patients at high risk of stroke and contraindication to anticoagulation in whom the excision of the LAA decreases thrombo-embolic risk. Moreover, the success rate after a single procedure in patients with persistent AF seems higher with MISAA compared with catheter ablation.
Figure 2
Left atrial cutplane (left atrial angiography overlay on fluoroscopic image, anteroposterior projection). The diagram shows the typical lesion sets around the pulmonary veins, drawn proximally to include the antral portion of all PVs. A line at the roof of the left atrium joins the two upper pulmonary veins. A line interrupting the left mitral isthmus joins the left inferior pulmonary vein and the lateral mitral annulus. Linear lesions are often required in persistent atrial fibrillation in order to organize atrial fibrillation or to interrupt macro-re-entrant atrial tachycardia.
Strategies for atrial fibrillation catheter ablation
Initial attempts at AF catheter ablation consisted of ablating triggers inside the PV 22,29,30; however, it was soon observed that RF injury inside the veins carried the risk of causing PV stenosis. 31,32 The ablation strategy, therefore, changed to a more proximal and large encircling of the PV at the antrum, to achieve electrical disconnection of all four PVs with less risk of PV stenosis and a better long-term outcome. 33
Further, substrate modification may be needed in some cases, especially in persistent AF, to restore and maintain sinus rhythm. Ablation of complex and fractionated electrograms, although controversial, is reported in most series to be beneficial in organizing the fibrillating process and in yielding better long-term outcome when compared with PVI alone. 34–37 Left atrial linear lesions between the two upper PVs and between the left lower PV and the mitral annulus when added to PV isolation also improved procedural and long-term outcome. 38,39 The added value of one or more of these steps in paroxysmal AF ablation is debated, as the increment in acute success was seen to be at the price of an increase in subsequent left atrial tachycardia and the need for additional ablation procedures. 40,41 However, in persistent AF, the combination of two or more of these strategies enhanced efficacy and was associated with a better long-term outcome (Figure2). 34,42–47 Other techniques advocated ablation of ganglionic plexi, as autonomous nervous system activity has been shown to be closely related to AF in some cases. 48
Current guidelines recommend that all patients undergoing catheter ablation for AF have at least electrical isolation of all four PVs. 49 This is usually sufficient to restore durable sinus rhythm in patients with paroxysmal AF and short arrhythmia episodes, whereas patients with longstanding persistent AF or with permanent AF often need extensive ablation, including complete lines, to achieve a satisfactory outcome. Others should have an intermediate approach to target AF substrate in trying and avoiding excessive ablation potentially leading to left atrial flutters or complications.
Ablation for paroxysmal atrial fibrillation
Catheter ablation successfully treats paroxysmal AF in 41–94% of patients, with most recent studies reporting success rates of >80% (Table2). 33,37,38,40,44,47,50–63 PV isolation alone in paroxysmal AF is reported to achieve durable sinus rhythm without the need for AADs in 59–93% of patients, 38,51,53,57,58,60,64,65 and the addition of linear lesions (roof or mitral lines) for patients with ongoing or inducible AF after PVI achieved long-term success in 82–91%. 38–40,47,52,54,59,60 Other studies have used hybrid techniques involving PV isolation and substrate modification with or without lines (Table2). When AF inducibility testing is performed and ablation is continued until AF can no longer be sustained, success rate can be increased to 91% to the cost of increased atrial lesions and increased number of procedures. 40 In a study exploring practices and results of catheter ablation for AF in centres worldwide between 1995 and 2002, the overall success rate of ablation for paroxysmal and persistent AF was 52% without the concomitant use of AADs and an additional 24% were controlled with a previously ineffective drug. 66 However since then, strategies have evolved and success rates in recently published studies have been higher.
Table 2
Catheter ablation for paroxysmal atrial fibrillation
Literature review, paroxysmal AF ablation. Randomized or non-randomized prospective studies including 50 or more patients per group and reporting results for paroxysmal and persistent AF separately. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; CFAE, complex and fractionated atrial electrograms.
aIncluding patients with persistent AF.
Table 2
Catheter ablation for paroxysmal atrial fibrillation
Literature review, paroxysmal AF ablation. Randomized or non-randomized prospective studies including 50 or more patients per group and reporting results for paroxysmal and persistent AF separately. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; CFAE, complex and fractionated atrial electrograms.
aIncluding patients with persistent AF.
Ablation for persistent atrial fibrillation
Pulmonary vein isolation alone to treat persistent AF was reported to achieve freedom from AF in 20–61% of cases, although some reported success rates of up to 95%, 67,68 and complex fractionated atrial electrogram ablation alone was reported to be successful in 9–85% (Table3). 33,35–37,43,45,47,55,64,69–71 For the majority with persistent AF however, ablation of PV targets seemed insufficient. 72 Strategies using a combination of approaches such as PV isolation, complex and fractionated atrial electrogram ablation, and linear ablation achieved higher success rates of 42–95% without AADs, with most centres reporting success in >70%. 34,42,44–47,50,54,73–78 Importantly, two or more procedures were often necessary in order to control persistent AF, and patients considering ablative treatment should be aware that approximately half require more than one session.
Table 3
Catheter ablation for persistent/chronic atrial fibrillation
Literature review, persistent AF ablation. Randomized or non-randomized prospective studies including 50 or more patients per group and reporting results for paroxysmal and persistent AF separately. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; CFAE, complex and fractionated atrial electrograms; L, left; R, right.
aIncluding patients with paroxysmal AF.
Table 3
Catheter ablation for persistent/chronic atrial fibrillation
Literature review, persistent AF ablation. Randomized or non-randomized prospective studies including 50 or more patients per group and reporting results for paroxysmal and persistent AF separately. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; SR, sinus rhythm; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; CFAE, complex and fractionated atrial electrograms; L, left; R, right.
aIncluding patients with paroxysmal AF.
Ablation vs. drugs studies
Seven studies directly comparing catheter ablation and drugs have confirmed the fact that sinus rhythm is better maintained following catheter ablation (Table4). A total of 763 patients were enrolled in these studies, 380 in the catheter ablation group and 383 in the AAD group. In an intention to treat analysis, catheter ablation resulted in atrial arrhythmia freedom in 79% compared with only 32% in the AAD group (P < 0.001). 52,79–84 Four studies enrolled only patients with paroxysmal AF, and catheter ablation achieved success in 81% without concomitant AAD therapy. 52,79–80 In comparison, AADs maintained sinus rhythm in only 29% (P < 0.001 vs. ablation in all four studies). Two other studies included paroxysmal and persistent AF, and success rate of ablation was 64% compared with 20% for AADs. 81,82 In patients with persistent AF only, AF freedom was achieved in 75% at 1 year in the ablation group, with 27% needing more than one procedure. In comparison, 55% in the AAD group had a favourable outcome. However, these results have to be interpreted taking into account the high cross-over rate in one of the studies, 83,84 and the small number of patients in the other. 84 However, given the important reduction in absolute and relative risk with ablation in all these studies, if one would wish to test the hypothesis in another study, only 15 patients per group would be needed to achieve 80% power with P < 0.05.
Table 4
Randomized trial ablation vs. anti-arrhythmic drug
Literature review on drugs vs. ablation for AF treatment. Results after 1-year follow-up. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; PM, pacemaker; SSS, sick sinus syndrome; AVN, atrioventricular node; Abl, ablation group.
Table 4
Randomized trial ablation vs. anti-arrhythmic drug
Literature review on drugs vs. ablation for AF treatment. Results after 1-year follow-up. AAD, anti-arrhythmic drug; PAF, paroxysmal AF; PsAF, persistent AF; PVI, pulmonary veins isolation; CPVA, circumferential pulmonary veins ablation; PM, pacemaker; SSS, sick sinus syndrome; AVN, atrioventricular node; Abl, ablation group.
In addition to being superior to AADs in maintaining sinus rhythm, catheter ablation resulted in better symptomatic relief and better exercise tolerance compared with drug treatment. 81 Improvement in quality of life scores occurred in both groups, but to a greater extent in the ablation group. 79,81 Atrial fibrillation burden was also decreased to a greater extent in patients treated by ablation, and improvement in exercise tolerance was greater following ablation compared with AAD therapy. 52 All these results, however, have to be interpreted with caution as the endpoint of AF freedom was imperfectly assessed in all of the studies since no continuous rhythm monitoring was used; rather, Holter monitoring and/or daily transtelephonic rhythm stripes were recorded randomly or as mandated by symptoms.
Atrial fibrillation ablation in patients with heart failure
The prevalence of AF in patients with heart failure is estimated to be between 10 and 50% and is associated with a 1.5 to 3-fold increase in mortality. 85,86 Atrial fibrillation contributes to the alteration in ventricular function by increasing heart rate, creating atrioventricular dyssynchrony, and impairing left atrial transport function, and by the irregularity of the heart rate. 87–90 Treatment of AF by catheter ablation has proved to be particularly beneficial in this population by increasing left ventricular function along with restoring sinus rhythm and alleviating heart failure symptoms. Ejection fraction was improved after ablation in a population with congestive heart failure and AF. 91 Importantly, the benefit was observed whether or not patients had concurrent structural heart disease and whether or not heart rate was adequately controlled prior to ablation, extending the advantages of sinus rhythm beyond the reduction in heart rate. 92 In PABA-CHF, 76% of patients with heart failure and AF undergoing AF ablation improved their ejection fraction compared with only 25% with atrioventricular junction ablation and biventricular pacing. 93 There is, therefore, evidence that sinus rhythm is desirable in patients with heart failure and that catheter ablation is effective in achieving it and improving the patient's overall condition.
Adverse events
It is difficult to determine the exact incidence of fatal or life-threatening arrhythmic events directly attributable to AADs in trials, since these events are rare, can occur any time over the course of therapy, and can also be caused by other factors. Nevertheless, in RACE, four patients in the rhythm control group died suddenly and three had life-threatening ventricular arrhythmia compared with none in the rate control group and in AFFIRM; although no significant difference in mortality was evidenced between the rate and rhythm control group, a sub-analysis revealed that AAD treatment was associated with a 49% increase in mortality. 1,3,5 The incidence of significant bradyarrhythmia during AAD treatment varied from 3 to 9% in different trials. 1,2,17,79 The 1-year incidence of adverse events attributable to amiodarone was, in one study, 0.6% for hepatic toxicity, 0.3% for peripheral neuropathy, 0.9% for hyperthyroidism, 1% for pulmonary toxicity, and 6% for hypothyroidsm. 94
Complications of catheter ablation procedures, on the contrary, are often more flamboyant and can be directly linked to the intervention. Mortality following catheter ablation of AF is one per thousand procedures according to a recently published international survey analysing cases from 162 centres worldwide over more than 10 years, from 1995 to 2006. 95 A similar survey reported in 2005 an overall complication rate of 6% for AF ablation procedures, including a 1:2000 risk of procedural death, 1.2% risk of tamponade, 1% risk of stroke or transient ischaemic attack, and <2% PV stenosis, with 0.6% developing symptoms. 66 Others reported higher rates of PV stenosis, up to 28%; however, severe reduction in lumen of >70% occurred in only 1–3% of patients. 96–99 In the presence of severe symptomatic PV stenosis, PV stenting was attempted with an acute angiographic success rate of 95%, and long-term patency of the PV was associated with the resolution of symptoms. 97,100 The most feared complication of catheter ablation, atrio-oesophageal fistula often leading to fulminant sepsis and death, is very rare. Its true incidence is difficult to establish with certainty, but was estimated to in 0.01%. 101 Different strategies are advocated to try and prevent this fatal complication, but their efficacy is difficult to evaluate because of the small number of events. Oesophageal temperature monitoring and opacification of the oesophagus with barium paste prior to the procedure have been used as a means of avoiding injury, and a recent publication reported that the use of conscious sedation was associated with significantly less endoscopic oesophageal lesions compared with the use of general anaesthesia. 102
Complications of each strategy, therefore, seem to occur at a similar rate; however, adverse events secondary to catheter ablation are more readily identified compared with those related to AADs, which are more insidious.
Health economy
Cost-effectiveness of catheter ablation for AF is difficult to determine and to generalize since differences in centres' experience, use of technologies, and rates of reimbursement are important factors in the calculation of costs and vary from centre to centre and from country to country; therefore, a unique model cannot account for all situations. 103 In France, studies suggested the cost of catheter ablation for symptomatic drug refractory paroxysmal AF to be lower than for medical therapy after 5 years, 104 whereas in Canada, catheter ablation for AF was deemed cost neutral compared with medical therapy within 2–4 years of the procedure for patients with symptomatic paroxysmal AF. 105,106 In the UK, catheter ablation for symptomatic paroxysmal AF was found potentially cost-effective on condition that the benefits in terms of quality of life improvement were maintained at 5 years, 107 and a recent review assessing cost-effectiveness found catheter ablation more effective, however more costly when compared with rate control treatment. 108 In the USA, cost-effectiveness was dependent on the underlying risk of stroke, the criteria being met in patients with a moderate risk but not in those at low risk. 109 Whether catheter ablation is cost-effective for patients in persistent AF will be answered by the Catheter Ablation for the Cure of AF-2 study, ongoing in 14 European centres. 110
Limitations
From these data, catheter ablation seems to be superior to AADs in restoring and maintaining sinus rhythm over the long term in patients with both paroxysmal and persistent AF. However, these conclusions have to be tampered by the following limitations: endpoints differed between ablation and AAD studies and among ablation studies themselves; most of patients in ablation studies were attempting second-line therapy as opposed to AAD trials: this could partly explain why the success rate of AADs in these latter trials was much lower than in comparative AAD trials, where a significant proportion was enrolled after a first episode. An important proportion of the studies on catheter ablation is non-randomized or single-centred. 108 Several techniques are advocated by different groups worldwide with variable success rates. The lack of uniformity in ablation techniques, in follow-up intensity, and in the way to report long-term outcome is a challenge when trying to interpret and compare results from different groups. Most data on catheter ablation of AF in the literature stem from a few high-volume centres which are overrepresented and may not reflect results obtained in other smaller centres. This statement also applies to the literature about AF ablation in patients with heart failure. Most studies report 1-year follow-up after ablation, which is rather short considering the nature of the disease in AF.
Conclusion
The available evidence supports the superiority of catheter ablation over medical therapy in the treatment of AF in terms of efficacy in maintaining sinus rhythm. Catheter ablation of AF should, however, be considered as a closed heart surgical procedure with all inherent potential of rare but debilitating complications. It should, therefore, be emphasized that there is consensus in the current practice guidelines to consider catheter ablation as a second line treatment for AF, after failure of medical therapy, and to reserve it for patients who are symptomatic. The future may hold a greater role for ablation, as we achieve better understanding of AF physiopathology, improve tools allowing faster, more efficient, and safer procedures, and as ongoing studies are conducted to assess whether there is a survival advantage with the ablative treatment of AF.
Funding
I.N. acknowledges financial support from St Jude Medical as a fellowship grant. M.W. acknowledges the financial support from the Department of Health via the National Institute for Health Research (NIHR) Comprehensive Biomedical Research Centre award to Guy's & St Thomas' NHS Foundation Trust in partnership with King's College London and King's College Hospital NHS Foundation Trust. I.N. received fellowship support from St Jude Medical.
Conflict of interest: none declared.
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Published on behalf of the European Society of Cardiology. All rights reserved. © The Author 2010. For permissions please email: journals.permissions@oxfordjournals.org
Published on behalf of the European Society of Cardiology. All rights reserved. © The Author 2010. For permissions please email: journals.permissions@oxfordjournals.org
Source: https://academic.oup.com/eurheartj/article/31/9/1046/591721
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