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Eur J Cardiothorac Surg 1998;13:629-636
© 1998 Elsevier Science NL

Venticular arrhythmia following successful myocardial revascularization: incidence, predictors and prevention

Department of Cardiac Surgery, Baptist Medical Center, Birmingham, AL, USA

Received 28 September 1997; received in revised form 16 March 1998; accepted 24 March 1998.

Corresponding author. Suite 300, Cardiac Surgery, 817 Princeton Avenue SW, Birmingham, AL 35211, USA. Fax: +1 151 2593870.

	Abstract

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Objectives: We estimated the risk of sudden cardiac death (SCD), from a spontaneous episode of ventricular arrhythmia (VT/VF), after a successful surgical myocardial revascularization (coronary artery bypass grafting; CABG) procedure. Predictors of these events were identified, and long term benefits of the prophylactic regimes, that were used to control these events, were evaluated. Methods: We selected 8642 consecutive patients, who had undergone an isolated and first time CABG procedure, between 1/3/1980 and 1/3/1995. A standard hazard function model (1) was used for statistical analysis. Efficacy of the prophylactic regimes, was examined in a group of 350 high risk patients, with a preoperative left ventricular ejection fraction 30% or less, who were recently operated since 1/1/1988. Electrophysiologic (EP) guided prophylaxis was used in 92 (26%) patients, who had survived a documented episode of SCD, and remaining 258 patients were maintained on antiarrhythmic medication on an empirical basis. A sequential EP evaluation was performed, when indicated. Results: During an early phase of hazard, which mainly lasted for up to 3 months after CABG, incremental risk factors were preoperative LVEF 30% or less (P=0.0007) and preoperative episodes of VT/VF (P=0.04). This phase was followed by a constant phase with a low risk of the events, which merged into a slowly rising late phase after 6 years. EP guided prophylaxis, reduced the risk of SCD in high risk patients (P=0.03). A sequential EP evaluation, helped to detect the problems of drug resistance and a cross over from non-sustained to sustained runs of VT/VF. Conclusions: Despite a successful CABG surgery, risk of VT/VF persists. A routine EP evaluation before and after a CABG procedure is recommended in all patients with a poor left ventricular function.

Key Words: Sudden cardiac death • Ventricular arrhythmias • Coronary artery bypass grafting

	Introduction

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Patients with ischemic heart disease, remain at a constant risk of sudden cardiac death, from a refractory episode of ventricular arrhythmia [1]. This risk is usually higher in patients with a poor left ventricular function [3] [4] [5] [6] [7], and increases after a surgical intervention, in postoperative period [8]. Surgical revascularization, is well known to control these unexpected terminal events, more effectively than the conventional medical therapy [2]. However, surgical revascularization reduces a subsequent risk of ventricular arrhythmias [2] [3] [4], but this response is unpredictable in most patients [2] [8]. In order to achieve an effective prophylaxis against these events, it is imperative to identify high risk patients, and maintain them on a specific antiarrhythmic prophylactic regime [3] [4] [8] [9] [10] [11]. In this retrospective study, an attempt has been made in this direction.

	Patients and methods

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
We reviewed medical records of 8642 consecutive patients. These patients had undergone an isolated, uncomplicated and a successful surgical myocardial revascularization procedure, between 1/3/1980 and 1/3/1995. Clinical details of these patients, and exclusions from this study are summarized in Table 1. Our objectives were to estimate a time related risk of sudden cardiac death, from a documented and a refractory episode of ventricular arrhythmia. We have included, only documented episodes of these events for analysis. Incremental risk factors of these terminal events, were also identified simultaneously. A standard hazard function model [1] was used, as outlined in Appendix B. The same method was used as outlined in Appendix C to identify a group of high risk patients. These patients were most likely to develop the events. Subsequently, a greater attention was focused on this group. All 350 patients in this group, underwent a standard screening procedure [5] [12] [13] [14], as outlined in Appendix D. This process enabled us to select 92 (26%) patients for electrophysiologic (EP) guided prophylaxis, who needed it most. The remaining 258 patients in this group, remained on antiarrhythmic medication on an empirical basis. Clinical differences between these cohorts of patients are outlined in Table 2. Details of EP guided prophylaxis with pharmacologic agents, or an automatic internal cardioverter and defibrillator (ICD) system [3] [4] [10] [15] [16], are outlined in Table 3. In order to evaluate the long term efficacy of these prophylactic regimes, event free survival curves were constructed and compared, as described in Appendix E.

Ischemic cardiomyopathy: cardiac dilatation caused by ischemic myocardial degeneration [17].

Successful surgical myocardial revascularization: hemodynamically stable outcome, following an optimum anatomical revascularization.

Monomorphic ventricular tachycardia: is ventricular tachycardia with uniform QRS morphology in Lead 1, aVf and V1.

Polymorphic ventricular tachycardia: ventricular tachycardia with change in axis, greater than 45° or altitude greater than 50% or both.

Sustained ventricular tachycardia: monomorphic or polymorphic ventricular tachycardia, lasting for more than 30 s, with a cardiac rate greater than 100 beats/min.

Standard programmed EP protocol: a standard program of SP stimulation was used, after discontinuation of antiarrhythmic medication and allowing a clearance for at least five half lives. During the protocol, patients may have experienced induced ventricular fibrillation, which was defined as a disorganized rhythm with hemodynamic instability, needing a direct current shock, or a sustained induced ventricular tachycardia, lasting for 30 s or more, needing a termination of the stimulus.

EP guided prophylaxis: pharmacologic agents were used which terminated induced and sustained ventricular arrhythmias. Drug resistant cases were managed with an implantation of an ICD system [3] [4] [11] [15] [16].

A sequential EP evaluation: this procedure was performed, when EP guided prophylaxis failed to control events or symptoms.

Follow up: all high risk patients were monitored at regular intervals following the procedure or when symptoms recurred. These patients underwent periodic monitoring or a sequential EP evaluation, and antiarrhythmic regimes were reviewed as indicated.

	Results

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Hazard function of sudden cardiac death and incremental risk factors
Throughout this series, 103 sudden cardiac deaths (SCD) occurred from 131 documented episodes of ventricular arrhythmias (VT/VF), in 8642 consecutive patients, following a successful surgical revascularization. Hazard function identified an early phase, followed by a constant phase, which merged into a late phase after 6 years. Early phase reached its peak at 3 months, and then declined rapidly. During this phase, patients were most susceptible to develop these unexpected terminal events (SCD, VT/VF). This phase was obviously influenced to some extent by inadequacies in myocardial protection or perioperative infarction, but on multivariate analysis, the variables which emerged as incremental risk factors were a preoperative left ventricular ejection fraction (LVEF) 30% or less (P=0.0007) and preoperative epidodes of ventricular arrhythmias (P=0.04) ( Fig. 1 ).

View larger version (26K): [in this window] [in a new window]   Fig. 1. Hazard function of sudden cardiac death (SCD) from a documented and a spontaneous episode of ventricular arrhythmia (VT/VF), following a successful myocardial surgical revascularization (CABG) procedure. Number of events and patients: SCD=103, VT/VF=131, CABG=8642. Beneficial effects of CABG reduced events for up to 6 years. During constant phase risk of events has remained higher than the expected risk of these events in average US population without ischemic heart disease.

Identification of high risk patients
In patients operated since 1/1/1988, a normogram was constructed as described in Appendix B. It confirmed that male patients, 60 years or older, were most likely to develop sudden cardiac death from ventricular arrhythmias, when their preoperative LVEF was 30% or less ( Fig. 2 ).

View larger version (24K): [in this window] [in a new window]   Fig. 2. Normogram showing a higher risk of sudden cardiac death in a male 60 years or older, when preoperative left ventricular ejection fraction was 30% or less. Numbers: LVEF<30%=350, LVEF>30%=3143. A disparity in NYHA grades between the populations was related to left ventricular function. Broken line represents demographically matched US population, without coronary artery disease.

Long term event free survival in high risk patients and efficacy of the prophylactic regimes
As described in Appendix E, both parametric and non-parametric methods were used, as appropriate. A comparative evaluation of the prophylactic regimes showed that EP guided prophylaxis, resulted in a better long term control of ventricular arrhythmias, and a significant reduction in the cumulative hazard of sudden cardiac death (P=0.03) ( Fig. 3 ).

View larger version (21K): [in this window] [in a new window]   Fig. 3. Cumulative hazard of sudden cardiac death from documented episodes of ventricular arrhythmias, in a high risk group of 350 patients with a left ventricular ejection fraction 30% or less, undergoing an isolated and first CABG procedure. Numbers: EP guided, 92; non-EP guided or empirical antiarrhythmic medication, 258; total deaths, 86; refractory ventricular arrhythmias, 55; episodes terminated by ICD, 11 (EP guided, 9; after a sequential EP testing, 2). Corresponding Kaplan Meier estimates of survival free from ventricular arrhythmias, excluding recurrent episodes were as shown in Table 4.

	Discussion

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

Incremental risk factors
As expected, and also reported earlier [2] [4] [6] [7] [8] [9] [10], our patients, who had developed poor left ventricular function prior to surgery, remained susceptible to sudden cardiac death, despite a successful surgical revascularization procedure. This may be attributed to the residual effects of a previous ischemic episode, inclusive of ischemic scarring, arrhythmogenic foci and reentry pathways [5]. These changes are not reversed by a surgical revascularization, and may continue to trigger ventricular arrhythmias, after a revascularization procedure [5]. Other incremental risk factors of the events, which have been identified are: a recent episode of myocardial infarction or ventricular arrhythmia prior to surgery, perioperative myocardial infarction, and a prolonged period of low cardiac output state postoperatively [5].

Screening of high risk patients and selection of patients for an invasive EP evaluation
As reported by others [2] [4] [6] [9] [10], risk of a sudden cardiac death was highest in our patients with poor left ventricular function. This risk is known to increase exponentially, when these patients acquire a tendency to develop sustained runs of ventricular arrhythmias [4] [9] [10]. In order to plan an effective prophylaxis, it is imperative to identify this cohort of patients. As recommended earlier [5] [12] [13] [14], we conducted an initial screening of our patients with poor left ventricular function (LVEF 30%). This process involved ECG/Holter or SAECG monitoring, as appropriate [5] [12] [14]. Finally, a cohort of patients was selected for an invasive EP evaluation, which needed it most. These patients clearly demonstrated short runs of ventricular arrhythmias or ventricular extrasystoles, which explained their previous non-fatal episodes of syncope or sudden cardiac death. As in previous studies [3] [4] [8] [9] [10] [11], financial constraints restricted us to use this selective approach, for EP evaluation. In these select patients, an invasive EP evaluation clearly differentiated their ability to develop sustained or non-sustained runs of ventricular arrhythmias [3] [4] [8] [9] [10] [11].

EP guided prophylaxis for sustained ventricular arrhythmias
In patients with this problem, an empirical administration of antiarrhythmic medication, invariably fails to prevent sudden cardiac death [4] [5] [15], and an EP guided prophylaxis is strongly recommended [4] [5]. Our patients with this specific problem, were maintained on specific antiarrhythmic drugs, which terminated induced and sustained runs of ventricular arrhythmias, on EP evaluation. It is a standard practice to implant an ICD system in pharmacologically resistant patients [2] [5] [16]. In this series, ICD implantation was preferred over ablative surgical procedures. This policy was influenced by low mortality and complication rate, which have been described for an ICD implantation. Unfortunately, hospital mortality for ablative surgical procedures has remained between 7 and 10% [19], and their higher failure rate may be attributed to problems in identification of arrhythmogenic foci and reentry pathways on an intraoperative EP mapping. According to a recent report, almost 2–3% deaths per annum, may occur following a successful ICD implantation [19]. This problem was averted in our patients, by an early detection and management of ICD related malfunctions and complications.

Prophylaxis for non-sustained ventricular arrhythmias
It is generally believed that non-sustained runs of ventricular arrhythmias are innocuous [4] [5]. Recently, this concept has been disputed, and a cautious approach to this problem has been advocated [10]. In accordance with this policy, we carefully monitored all our patients with this problem. In select patients, a sequential EP evaluation enabled us to detect a crossover from non-sustained to sustained runs of ventricular arrhythmias. These patients were successfully managed with an ICD implantation.

Routine versus selective EP guided prophylaxis in patients with poor left ventricular function
Recently, some researchers [5] [20] have advocated a routine pre- and postoperative EP evaluation, in all patients with a poor left ventricular function. This approach, is expected to benefit most, if not all patients, who are susceptible to develop terminal episodes of ventricular arrhythmias, after a successful surgical revascularization. Unfortunately, financial constrains and lack of facilities, often restrict a liberal use of EP evaluation. So far, it has not been possible to determine the cost effectiveness of this approach. Therefore, most centers [4] [9] [15] [16] [19] [20], have continued to use a selective approach, as outlined in this report. Unfortunately, this approach covered only 26% of our patients with a poor left ventricular function. This selective approach, obviously fails to protect a number of patients with a potential, yet an unproven risk of sudden cardiac death [18] [19]. Our study also shows that a routine use of pre- and postoperative EP evaluation, in our patients with a poor left ventricular function, could have prevented a number of unexpected deaths.

Arrhythmia prophylaxis in patients with a preserved left ventricular function
These patients are known to have a much lower risk of sudden cardiac death, as compared with patients with poor left ventricular function [2] [4] [10]. Nonetheless, this risk is still higher than the expected risk of these events, in a demographically matched population without ischemic heart disease. So far, prophylactic guidelines have not been defined for these patients. A multicentric clinical trial, which is in progress, may provide a useful input in this direction. This trial may recommend a routine implantation of an ICD patch or system, in all patients, at the time of their first surgical revascularization [18]. It remains to be seen, whether this fail safe approach would be accepted as a standard practice, in future.

	Conclusions

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Despite a successful myocardial revascularization procedure, risk of a spontaneous and an intractable episode of ventricular arrhythmia persists. This risk is particularly higher in patients with a poor left ventricular function. This risk may be attributed to the following facts: (1) inability of a CABG procedure to reverse the ischemic damage, already caused by a previous episode of ischemia or infarction, (2) the progressive nature of coronary artery disease, and (3) a palliative nature of the revascularization procedures, which have a finite life. A routine use of electrophysiologic evaluation, before and after a CABG procedure is highly recommended, in patients with a poor left ventricular function. A sequential EP evaluation is helpful in select patients, for the detection of the problems of drug resistance and a cross over from non-sustained to sustained ventricular arrhythmias.

	Appendix A. Conference discussion

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Joao Melo (Carnaxide, Portugal): You have shown an improvement of 0.01/month events after EP-studied patients were treated according to whatever was the decision. But was there any difference between those that had only the antiarrhythmic treatment and those that had ICD?

Dr Kaul (Birmingham, Alabama): A comparative evaluation of these prophylactic measures is only available in patients with a global LVEF<30%. Follow up was complete. We did not include patients with LV aneurysm and other high risk patients as they required a separate protocol, including intraoperative EP mapping and almost a routine preop EP evaluation. When patients demonstrated life threatening sustained VT/VF on EP evaluation, they were started on specific antiarrhythmic drugs that terminated these events on examination. Only drug resistant cases received ICD implantation. Major disadvantages on long term antiarrhythmic drug prophylaxis were: (1) development of drug resistance especially when procainamide was used, and (2) sometimes a crossover from a non-sustained to sustained VT/VS status. These problems were identified on sequential EP evaluation and successfully managed with ICD implantation. Despite initial differences in patient selection, ICD implantation resulted in a more durable and reliable prophylaxis. Hospital mortality for ICD implantation was nil, but some patients did develop malfunction or complications and required ablative surgical procedures. Because of obvious limitations, I am unable to substantiate this comparison with statistical evidence. When we translate event free survival benefits of EP guided therapy into Kaplan Meir estimates ( Fig. 2), the advantages of EP guided therapy are obvious and significant.

In this retrospective study, we have taken only documented episodes of the `events' into consideration. A prospective analysis is likely to reveal a much higher incidence of SCD due to spontaneous VT/VF following CABG surgery and a greater need of antiarrhythmic prophylaxis.

Dr Melo: And what is your approach if you have a patient with an ejection fraction over 30% but you suspect that you have some sort of arrhythmia problem?

Dr Kaul: Well, 30% is not a cut-off point.

Dr Melo: Yes, of course.

Dr Kaul: It very much depends also on the general picture, the previous history or evidence of coexisting problems such as cerebrovascular disease, systemic hypertension, prolapsing heart valve, obstructive or dilated cardiomyopathy, etc. When coexistent lesions are capable of initiating ventricular arrhythmia or manifesting a simulated clinical picture, an appropriate management of these additional problems would become necessary. In patients with isolated CAD and a LVEF>30%, suspicion of arrhythmia should be confirmed with ECG/Holter's/SAECG monitoring. Patients demonstrating a documented evidence of runs of VES/VT/VF or a high VES count/h, should undergo invasive EP evaluation and receive EP guided prophylaxis, as described for patients with a LVEF less than 30%. These patients are more likely to withstand an ablative surgical procedure. I believe, most of us would agree with this approach. However, a multicentric randomized clinical trial is in progress which is evaluating the benefits and the limitations of a routine implantation of an ICD system, at the time of CABG. So far, this approach has not shown a significant improvement in patient survival, but more information should become available next year. This trial may recommend: (1) implantation of a full ICD system or (2) just leads at the time of a routine CABG. This complex question needs to be resolved with a multicentric consensus, based on scientific evidence.

	Appendix A. Statistical analysis

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Initial analysis: the usual contingency tables and methods were used to establish the differences, between the variables listed in Table 1Table 2, prior to multivariate analysis.

Hazard function and incremental risk factors: a generic hazard function model (1) was utilized, to determine a time related risk of sudden cardiac death, from documented episodes of ventricular arrhythmias, at all points in this series. Incremental risk factors, which increased the risk of these events, were identified simultaneously ( Fig. 1). Determinants of the events (sudden cardiac death, ventricular arrhythmias), were identified by multivariate analysis for each component phase of hazard, using same variables as listed. These variables were entered into the model sequentially, by means of a direct and non-automated technique. Variables which passed the likelihood ratio test with a P-value 0.05 or less, were retained in the model. Variables with a P-value 0.10 or less, were reexamined for each phase of hazard. Variables: age (3rd to 6th decade, finally 60 years or under vs. over 60 years; gender (male/female); hypertension (yes/no); diabetes (yes/no), recent (3 months or less prior to surgery); cigarette smoking (yes/no); a family history of coronary artery disease (yes/no); abnormal lipids or hyperlipidemia (yes/no); New York Heart Association (NYHA) Class III–IV (yes/no); stable angina class IV (yes/no); unstable angina (yes/no); recent myocardial infarction (yes/no); recent episode of a ventricular arrhythmia (yes/no); recent episode of CHF (yes/no); sudden cardiac death (yes/no); syncope (yes/no); ischemic and dilated cardiomyopathy (yes/no); preoperative intra aortic balloon pump support (IABP) (yes/no); triple coronary vessel disease (yes/no); left main stem or aorto-osteal coronary artery disease, with a minimum of 50% stenosis (yes/no); preoperative left ventricular ejection fraction (LVEF) 30% or less (yes/no); retrograde cardioplegia (yes/no); perioperative myocardial infarction (yes/no); IABP support for weaning off bypass (yes/no).

A graphic representation of hazard into phases, incorporated multivariate equations and corresponding incremental risk factors, as shown in Fig. 1.

Early phase: d=0, P=0.1001, v=1.421, intercept, 1042. Incremental risk factors: age 60 years or older P=0.06, male gender P=0.08, preoperative CHF and ischemic cardiomyopathy P=0.01, left ventricular ejection fraction 30% or less prior to surgery P=0.0001, preoperative episodes of ventricular arrhythmias P=0.04.

Late phase: ischemic cardiomyopathy P=0.07. In the domain of constant phase, results were influenced by the beneficial effects of surgical revascularization, e.g. an improvement in the LVEF and NYHA clinical grades, and in the domain of late phase by progression or a fresh onset of ischemic cardiomyopathy.

	Appendix A. Identification of high risk patients

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
For this purpose, a search was conducted in patients, who were operated since 1/1/1988. From this date onwards, follow up was complete, a uniform protocol was used for myocardial protection, and electrophysiologic (EP) evaluation was regularized. A multivariate solution was sought to identify this group of patients. It involved, examination of effect/effects of the variables/combination of variables, on the events (sudden cardiac death, ventricular arrhythmias), while keeping other variables on hold. By a process of elimination, finally a group of high risk patients were identified, comprising of 350 male patients, aged 60 years or older, with a preoperative LVEF 30% or less ( Fig. 2). Demographic characteristics of this group, matched with the majority of patients in this series, and preoperative episodes of ventricular arrhythmias, mainly occurred in patients with poor left ventricular function. For these reasons, this group of patients was accepted for a detailed analysis.

	Appendix A. Screening of high risk patients and selection of patients for electrophysiologic evaluation

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
All 350 high risk patients, as identified in Appendix C, underwent a standard screening procedure. This process involved a minimum of 24 h continuous electrocardiographic (ECG) monitoring in the hospital, followed by Holter's monitoring in ambulant state, for up to 5 days. In all recordings, arrhythmia mode was preferred over symptomatic mode. Information was supplemented by recording late potentials by a signal averaged ECG (SAECG) monitoring, especially in patients with a recent history of myocardial infarction or ischemia. A comprehensive analysis of all recordings, enabled us to concentrate on a cohort of 110 patients, who demonstrated runs of ventricular arrhythmias, extrasystoles or a high ventricular premature beats per hour on monitoring. These recordings explained their previous episodes of syncope or sudden cardiac death. Of these, 92 (26%) patients were selected for EP evaluation, who had survived a documented episode of ventricular arrhythmia. A complete breakdown of 110 patients who survived/experienced sudden cardiac death, along with their main presenting features was as follows: pre- and postoperative VT/VF=38/47, postoperative VT/VF=12/15 and late SCD=42/48.

The remaining 258 patients, who failed to demonstrate runs of VT/VF or ventricular extrasystoles on monitoring, or those who failed to respond were not selected for EP evaluation. Nonetheless, these patients remained under a close supervision, underwent a periodic monitoring with ECG/Holter/SAECG, as indicated, and were maintained on antiarrhythmic medication on an empirical basis.

	Appendix A. Long term event free survival with prophylactic regimes in high risk patients

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 
Both parametric [1] and non-parametric (Kaplan Meir) methods were used, as appropriate. Kaplan Meir method by its strict censorship, excludes patients from the model after an event. This method did not permit retention of our patients, who survived an episode of ventricular arrhythmia, through a pharmacologic or electronic intervention. In view of these limitations, we have used Kaplan Meir predictions to examine survival curves free from ventricular arrhythmias, and parametric method (1), to compare the cumulative hazard of sudden cardiac death ( Fig. 3).

	References

Top Abstract Introduction Patients and methods Results Discussion Conclusions Appendix A. Conference... Appendix A. Statistical... Appendix A. Identification of... Appendix A. Screening of... Appendix A. Long term... References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Barry L. Fields Lee S. Riggins David A. Wyatt Christopher R. Jones Permission Requests Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Kaul, T. K. Articles by Jones, C. R. Search for Related Content PubMed PubMed Citation Articles by Kaul, T. K. Articles by Jones, C. R.