Spontaneous Initiation of Atrial Fibrillation by Ectopic Beats Originating in the Pulmonary Veins
Michel Haïssaguerre, M.D., Pierre Jaïs, M.D., Dipen C. Shah, M.D., Atsushi Takahashi, M.D., Mélèze Hocini, M.D., Gilles Quiniou, M.D., Stéphane Garrigue, M.D., Alain Le Mouroux, M.D., Philippe Le Métayer, M.D., and Jacques Clémenty, M.D.
Background Atrial fibrillation, the most common sustained cardiacarrhythmia and a major cause of stroke, results from simultaneousreentrant wavelets. Its spontaneous initiation has not beenstudied.
Methods We studied 45 patients with frequent episodes of atrialfibrillation (mean [±SD] duration, 344±326 minutesper 24 hours) refractory to drug therapy. The spontaneous initiationof atrial fibrillation was mapped with the use of multielectrodecatheters designed to record the earliest electrical activitypreceding the onset of atrial fibrillation and associated atrialectopic beats. The accuracy of the mapping was confirmed bythe abrupt disappearance of triggering atrial ectopic beatsafter ablation with local radio-frequency energy.
Results A single point of origin of atrial ectopic beats wasidentified in 29 patients, two points of origin were identifiedin 9 patients, and three or four points of origin were identifiedin 7 patients, for a total of 69 ectopic foci. Three foci werein the right atrium, 1 in the posterior left atrium, and 65(94 percent) in the pulmonary veins (31 in the left superior,17 in the right superior, 11 in the left inferior, and 6 inthe right inferior pulmonary vein). The earliest activationwas found to have occurred 2 to 4 cm inside the veins, markedby a local depolarization preceding the atrial ectopic beatson the surface electrocardiogram by 106±24 msec. Atrialfibrillation was initiated by a sudden burst of rapid depolarizations(340 per minute). A local depolarization could also be recognizedduring sinus rhythm and abolished by radio-frequency ablation.During a follow-up period of 8±6 months after ablation,28 patients (62 percent) had no recurrence of atrial fibrillation.
Conclusions The pulmonary veins are an important source of ectopicbeats, initiating frequent paroxysms of atrial fibrillation.These foci respond to treatment with radio-frequency ablation.
Atrial fibrillation is the most common of all sustained cardiacarrhythmias, with the prevalence increasing with age to up to5 percent in persons more than 65 years of age, and it is amajor cause of stroke.1,2,3 Experimental studies and human surgicalmapping studies have shown that atrial fibrillation is perpetuatedby reentrant wavelets propagating in an abnormal atrial-tissuesubstrate.4,5,6,7,8 Complex approaches have been developed tointerrupt wavelets, including extensive surgical or, recently,catheter-mediated atriotomy.9,10,11,12,13,14,15,16,17,18,19,20,21There are, however, no data about the spontaneous initiationof atrial fibrillation. The triggers of atrial fibrillationmay be focal targets for ablative therapy. We investigated themode of initiation of spontaneous paroxysms of human atrialfibrillation by atrial ectopic beats, the characteristics ofthese triggering beats, and the effects of local ablation withradio-frequency energy.
Methods
Characteristics of the Patients
The study population consisted of 45 patients enrolled consecutively(Table 1) who met the following criteria: the patient had tohave atrial fibrillation resistant to more than two drugs, therehad to be at least one episode of atrial fibrillation everytwo days, the patient had to be receiving anticoagulant treatment,the patient had to have frequent isolated atrial ectopic beats(more than 700 per 24 hours), and the patient had to provideinformed consent. The protocol was approved by the hospital'ssafety committee. Antiarrhythmic drugs were discontinued twoto five days before hospitalization; amiodarone was being takenby nine patients.
The patients were monitored by telemetry throughout their hospitalstays. Before ablation, atrial fibrillation occurred daily in39 patients and every two days in the other 6 patients, witha mean (±SD) duration of 344±326 minutes per 24hours. Twelve-lead electrocardiographic recordings were obtainedto document the morphologic features of the ectopic beats. In37 patients, at least one instance of initiation of sustainedatrial fibrillation lasting more than one minute was documented:the ectopic beat initiating atrial fibrillation had a shortcoupling interval (a P-on-T pattern) and morphologic featuressimilar to those of isolated ectopic beats. Their identicalorigin was confirmed later by intracardiac mapping data.
Electrophysiologic Study
Oral anticoagulants were replaced on admission by either subcutaneousor intravenous heparin to maintain a partial-thromboplastintime of 60 to 90 seconds (control, 30 seconds). Heparin wasstopped four to six hours before ablation, since transseptalcatheterization was sometimes required.
Three multielectrode catheters were introduced percutaneouslythrough the femoral veins: one quadripolar roving ablation catheterwith a thermocouple and a 4-mm tip, one catheter in the rightatrial appendage (for right atrial and right-pulmonary-veinfoci) or coronary sinus (for left-pulmonary-vein foci) to providestable reference electrograms during mapping, and one catheterfor stimulation.22,23 In three patients, two roving catheterswere used to map two pulmonary veins simultaneously. Surfaceelectrocardiographic leads (I, II, III, and V1) and bipolarintracardiac electrograms filtered at 30 to 500 Hz were recordedwith a polygraph (Midas, PPG Biomedical Systems, Lenexa, Kans.).
Stimuli were adjusted to be twice the diastolic threshold and2 msec in duration. If the arrhythmia did not spontaneouslydevelop during electrophysiologic monitoring or was not sufficientlysustained, physiologic procedures (e.g., Valsalva's maneuveror carotid-sinus massage), atrial pacing, pharmacologic agents(e.g., isoproterenol, adenosine triphosphate, digoxin, propranolol,or verapamil), or all three methods were used.
Localization of Arrhythmogenic Triggers (Atrial Ectopic Beats)
The preliminary study involved intracardiac mapping of isolatedectopic beats. The ectopic focus was localized according tothe earliest atrial activity relative to the reference electrogramor the onset of the ectopic P wave. Mechanically produced beatswere prevented by avoiding manipulation of the catheters duringthe recordings, and such beats were excluded from the analysisby comparing the electrocardiographic pattern and intracardiacsequence with the confirmed spontaneous ectopic beats. If nosharp bipolar activity was recorded in the right atrium earlierthan 10 msec before the onset of the ectopic P wave, the ectopicbeats were considered to have originated in the left atrium.Direct mapping of the left atrium and pulmonary veins was performedthrough a patent foramen ovale (in six patients) or by meansof transseptal catheterization. In the anteroposterior view,the pulmonary-vein ostia are situated on both sides of the spineand can be engaged by applying clockwise torque to the shaftof the catheter. The role of ectopic beats in the initiationof atrial fibrillation was confirmed by on-site recording ofa paroxysm of fibrillation.
Ablation Procedure
No heparin was administered for ablation in the right atrium.For the left atrium, an intravenous dose of 0.5 mg of heparinper kilogram of body weight was administered during ablation,followed by an infusion to maintain a partial-thromboplastintime of 60 to 90 seconds. The sedatives midazolam and nalbuphinewere administered intravenously to control pain.
Ablation was performed at the site with the earliest recordedectopic activity. To minimize the risk of clot formation, temperature-controlledradio-frequency energy was delivered at a target temperatureof 70°C in the right atrium or 55 to 60°C in the leftatrium between the catheter electrode and a patch electrodemeasuring 575 cm2 for 60 to 120 seconds, except when there wasa rise in impedance.24,25
Subcutaneous heparin was administered after ablation to maintainthe partial-thromboplastin time. Successful ablation was definedas the elimination of atrial triggers during the 60 minutesafter ablation and the absence of the morphologic features ofthe targeted ectopic beats during the subsequent eight dayswithout a need for antiarrhythmic drugs.
Telemetry and 24-hour Holter monitoring were performed continuously,and the data were monitored by nurses to identify the cumulativeduration of atrial fibrillation and the duration of fibrillationduring each hour. The patients were discharged and given oralanticoagulants for at least three months but no antiarrhythmicdrugs. Late follow-up consisted of visits to the hospital andHolter recordings every three months. Any undocumented but suggestivesymptoms were attributed to atrial fibrillation.
Statistical Analysis
Continuous variables were expressed as group means ±SDand were compared with the use of the Kruskal–Wallis test.Statistical significance was considered to be demonstrated bya two-tailed P value of less than 0.05.
Results
Origin of Atrial Triggers (Ectopic Beats)
A single point of origin of ectopic beats was identified in29 patients, two were identified in 9 patients, three were identifiedin 6 patients, and four in 1 patient, for a total of 69 ectopicfoci. Ectopic beats originated in atrial muscle ("atrial foci")in 4 patients (in the right atrium in 3 and the posterior leftatrium in 1) and in the pulmonary veins ("venous foci") in 41patients (a total of 65 foci [94 percent]): 31 foci in the leftsuperior, 17 in the right superior, 11 in the left inferior,and 6 in the right inferior pulmonary vein (Figure 1). The venousorigin of the earliest ectopic activity was demonstrated in23 patients by the radiographic position of the mapping catheter,which was superimposed on the lungs and was outside the cardiacsilhouette, and by confirmatory angiographic visualization.
Figure 1. Diagram of the Sites of 69 Foci Triggering Atrial Fibrillation in 45 Patients.
Note the clustering in the pulmonary veins, particularly in both superior pulmonary veins. Numbers indicate the distribution of foci in the pulmonary veins.
Characteristics of Triggering Ectopic Beats Arising in the Pulmonary Veins
The effective mapping of venous foci required multiple proceduresbecause of two major problems. First, the spontaneous occurrenceof ectopic beats and paroxysms of atrial fibrillation was unpredictable,and provocative procedures were not consistently effective.Second, sustained atrial fibrillation lasting for minutes orhours required either waiting periods for spontaneous interruptionor cardioversion. In five patients, there were no isolated ectopicbeats during mapping, because each ectopic beat set off atrialfibrillation. Venous foci exhibited the characteristic electrophysiologicpatterns described below.
Activity during Ectopy
The earliest local activity was traced to a point 2 to 4 cmwithin the main pulmonary vein or one of its proximal branches,and depolarization was marked by a "spike" (activity of sharponset and short duration as measured electrographically) precedingthe onset of the ectopic P wave by 106±24 msec (range,40 to 160) (Figure 2). The P wave was not distinct in six patientsin whom only the reference electrogram was used for mapping.The spike was localized, and its amplitude rapidly decreased,when the catheter tip was turned or moved a few millimeters.Bystander or far-field activity from contiguous branches couldbe distinguished by temporal delay or lower amplitude (<0.1mV). The spike occurred earliest deep in the vein and progressivelylater toward the ostium and the left atrial exit, resultingin distal-to-proximal venous activation during multipolar recordings(Figure 2). The amplitude of the unipolar electrograms of thespikes (<0.5 mV) was too low for morphologic analysis.
Figure 2. Angiogram of a Left Inferior Pulmonary Vein Depicting the Source and Exit of Ectopic Activity.
The electrogram showed characteristic changes in timing depending on the position of the recording catheter in the specific pulmonary vein. With an increasingly distal catheter position (toward the source), the spike was recorded progressively later during sinus rhythm (left-hand panel, arrows) and correspondingly earlier during ectopic activity (arrowhead). Conversely, in a proximal position at its exit into the left atrium (right-hand panel), the spike was not as delayed during sinus rhythm (arrows) nor as precocious during ectopic activity (arrowhead). The application of radio-frequency energy at the source of ectopic activity eliminated the local spike during sinus rhythm and ectopic beats and atrial fibrillation on a short-term basis. The dotted lines mark the onset of the ectopic P wave, and 1–2 and 3–4 are bipolar recordings from the distal and proximal poles of the mapping catheter. A indicates near-field atrial activity. The radiograph (center panel) shows the position of electrographic recordings inside the pulmonary vein at the source and exit.
A second electrographic component with a slow deflection (depolarizationrate [dv/dt], <0.5 mV per msec) reflecting later left atrialactivation was temporally distinct from the spike inside thevein and then approached and became continuous with the spikeat the ostium. The conduction time from the venous spike tothe activation of the left atrium increased progressively asthe coupling interval of the spike spontaneously shortened andwhen there were repetitive spike discharges. Nonconducted spikes(those confined within the vein) were recorded in 21 patients.They were more closely coupled with the previous beat than theconducted spikes (183±29 msec vs. 207±29 msec,P=0.03), and a threshold coupling interval below which the spikewas isolated could be identified in 19 patients.
Initiation of Atrial Fibrillation
Between one and eight instances of spontaneous initiation ofatrial fibrillation were recorded in 36 patients. Two patientswith atrial foci had atrial fibrillation induced after irregularatrial tachycardia, one with a mean cycle length of 230 msecand the other with a mean cycle length of 250 msec. In 34 patientswith venous foci, the initiation of atrial fibrillation wasdocumented for 45 of 58 foci with the use of a catheter in theappropriate vein. Atrial fibrillation was initiated by a singlefocal discharge in 3 patients (including 2 with structural heartdisease), a short burst of two or more repetitive focal dischargesin 40, and both mechanisms in 2 (Figure 3). Repetitive focaldischarges had irregular cycle lengths, ranging from 110 to270 msec, with a mean of 175±30 msec (340 per minute).Five foci discharged only in bursts, with each burst producingatrial fibrillation. The coupling interval from the last sinusbeat to the initial spike did not differ significantly betweenectopic beats that led to atrial fibrillation and those thatwere isolated (212±34 msec vs. 216±34 msec). Continuouselectrical activity could be recorded in the pulmonary veinduring the interval between successive spikes but not duringthe period preceding the first spike.
Figure 3. Two Examples of the Onset of Atrial Fibrillation from Foci in a Right Inferior Pulmonary Vein and a Left Superior Pulmonary Vein.
The electrogram with the pulmonary-vein spike is the terminal part of a two-component electrogram obtained during sinus rhythm. In the upper panel, a burst of five spikes (asterisks) with a mean cycle length of 170 msec induced continuous electrical activity in the right inferior pulmonary vein (RIPV), with coarse atrial fibrillation on the surface electrocardiogram. The coupling interval of the first spike was 265 msec. In the bottom panel on the left, a sinus beat (with a terminal spike) was followed by an isolated atrial ectopic beat (asterisk) at a coupling interval of 240 msec. The electrogram of the ectopic beat characteristically shows temporal reversal, with the rapid deflection spike preceding the lower-amplitude, slower far-field atrial activity. On the right, in the same patient, a train of spike discharges (asterisks) at a cycle length of 160 msec sets off atrial fibrillation. The spike discharges are also characterized by temporal reversal but exhibit a progressively prolonged conduction time to the atria. The coupling interval of the first spike on the right (240 msec) is identical to that of the isolated ectopic beat on the left. LSPV denotes left superior pulmonary vein, and U unipolar left atrial activity.
In nine patients, no spontaneous initiation of atrial fibrillationcould be documented during mapping. However, all nine had frequentisolated ectopic beats originating from a single focus (atrialin two patients and venous in seven, all with similar characteristics)and previous electrocardiographic documentation of the roleof these beats in initiating atrial fibrillation.
Activity during Sinus Rhythm
The spike could also be recognized during sinus rhythm in theterminal portions of local potentials after left atrial activity,and it occurred progressively later inside the vein, which isthe opposite of the sequence during ectopy (Figure 2). Multiplespikes were recorded at the ostia, particularly those of thesuperior veins. Similar (though less complex) electrograms couldalso be recorded in other nonarrhythmogenic pulmonary veins(those not giving rise to ectopic beats), indicating physiologicactivation of muscular left atrial tissue extending into theveins.26,27
Radio-Frequency Ablation
The four ectopic foci mapped to atrial muscle outside the pulmonaryveins exhibited the earliest activity — 35 to 45 msecbefore the onset of the ectopic P wave — implying a shortconduction time to the rest of the atrium. They were ablatedwith a median of 3 and a mean of 4.5±2 applications ofradio-frequency energy in one session.
The ablation of venous foci was performed at the earliest siteof the maximal amplitude of the spike during conducted or nonconductedectopic beats. As shown in Table 2, two sessions were requiredfor 25 patients and three sessions were required for 6 becauseof a recurrence after ablation or the detection of new foci.All but one recurrence occurred within three days of the initialprocedure. A mean of 5±5 and a median of 4 applicationsof radio-frequency energy were required for each focus.
Table 2. Outcome of In-Hospital Ablation According to Location of Focus.
No serious side effects were observed during these procedures.Cough was induced in some patients by applications of radio-frequencyenergy in the left superior veins near the bronchi and requiredthe cessation of the delivery of radio-frequency energy or areduction in power. Pain was sometimes severe, requiring additionaldoses of nalbuphine.
Electrograms recorded at the sites of successful ablation of57 venous foci showed the disappearance of the local spike duringsinus rhythm in 44 of the foci, an intermittent spike (everytwo or three beats) in 3, and dissociation from atrial activityas a slow automatic rhythm in 2 (Figure 4). At eight sites,the spike persisted, but with a lower amplitude and a delayof 10 to 50 msec.
Figure 4. Effects of Successful Radio-Frequency Ablation within the Superior Pulmonary Veins in Two Patients.
The tracings in the upper panel were recorded in a patient with dilated cardiomyopathy. Before ablation (left-hand side), a multicomponent electrogram was recorded in the right superior pulmonary vein (RSPV) with a terminal spike (asterisk). After ablation at this site (right-hand side), the spike disappeared. The tracing in the lower panel shows an example of ablation within the pulmonary vein resulting in slow and dissociated automatic spike activity in the left superior pulmonary vein (LSPV), marked by asterisks.
After ablation the angiograms of the pulmonary veins of 23 patientswere unremarkable except for a luminal irregularity (possiblya small thrombus) in 1 patient. Twenty of the sites of successfulablation were located at or near a branching point.
Follow-Up
Successful ablation of ectopic foci in the hospital was achievedin 38 patients. The Holter recordings of these patients showeda decrease from 4377±3629 to 98±91 ectopic beatsper 24 hours. Two patients had a recurrence of atrial fibrillation,whereas 36 patients had no recurrences during hospitalization,including the 9 patients without initiation of atrial fibrillationduring the ablation procedure. Ablation of the focus was unsuccessfulin seven patients, and all had recurrences of atrial fibrillationin the hospital.
During a mean follow-up period of 8±6 months (median,7), atrial fibrillation was eliminated completely in 28 patients(62 percent) without the use of drug therapy. Seventeen patientshad recurrences of atrial fibrillation, including those whohad early failures, and recurrences of ectopy were documentedin 12 of these patients during hospitalization or follow-up.
Discussion
This study indicates that the vast majority of atrial prematurebeats that initiate frequent paroxysms of atrial fibrillationoriginate in the pulmonary veins. These foci trigger atrialfibrillation with a burst of rapid discharges and respond tolocal radio-frequency ablation with a catheter.
The pulmonary veins were identified as major sources of atrialtriggers (ectopic beats) by means of intracardiac mapping, fluoroscopy,and angiographic imaging. Such venous foci were previously observedin a few patients who underwent atrial ablation for paroxysmalatrial fibrillation.20 In our study of patients who had notpreviously undergone ablation for atrial fibrillation, 94 percentof the atrial triggers originated in the pulmonary veins. Thisprevalence was similar to that in the subgroup of patients withstructural heart disease, but a larger series is needed to confirmthis result.
All the patients were enrolled because they had frequent anddrug-resistant paroxysmal atrial fibrillation, and the highprevalence of foci in the pulmonary veins may therefore reflectan anatomical site or mechanism that is particularly arrhythmogenicand resistant to conventional drug therapy rather than the trueprevalence in the general population with atrial fibrillation.In some patients, however, isolated ectopic beats could notbe recorded during mapping, because of long-lasting atrial fibrillationrequiring cardioversion, because no such beats were present,or both. This suggests that our methods and results could beapplied to a broader range of clinical situations with the useof more reliable provocative procedures and simultaneous multielectrodemapping.
The pulmonary-vein foci exhibited unique characteristics, includingdeep venous origin, unpredictable firing, and complex, delayedconduction to the left atrium with frequent ectopic beats confinedto the vein. A similar arrhythmia has been previously documentedbetween the superior vena cava and the right atrium —again in a great vein–atrial junction.28 The deep venousorigin contrasts with the juxtaostial origin of conventionalleft atrial tachycardias, and the long conduction time indicateseither discontinuous conduction or a tissue several centimeterslong, since the morphologic features of the spike indicate arapidly conducting structure. A long conduction time was alsoreproduced by local venous pacing, but the effects of stimulationthrough pacing therapy have not been explored.20
The recording of spikes during sinus rhythm in other pulmonaryveins reflects the physiologic activation of muscular bandsextending from the left atrium to the venous wall with complexpathways.26,27,29,30 The predominant distribution of foci inthe superior veins matches the dominant anatomical pattern ofthese atrial extensions.29 The reasons why pulmonary veins becomearrhythmogenic are unknown. However, their architectural topographycan accommodate various electrophysiologic mechanisms, notablyautomaticity, as indicated by dissociation after ablation intwo patients, and reentry, as suggested by continuous activitybetween subsequent spikes. In contrast, the first spike wasapparently linked to the previous sinus beat without there beingany intervening activity, suggesting triggered automaticityas a possible mechanism.31 In perfused dog hearts, abnormalautomaticity and various conduction disturbances have been demonstratedin the musculature of thoracic veins.28,29,30 In the literature,there are no data pertaining to the spontaneous initiation ofatrial fibrillation in humans or animals, but a recent preliminaryreport indicates the arrhythmogenic role of pulmonary veinsin dogs with congestive heart failure.32
In our patients, a train of repetitive rapid discharges (rate,340 per minute) initiated atrial fibrillation, which then continuedindependently. Atrial fibrillation was in fact the result ofthe abrupt transformation of apparently benign isolated ectopicbeats into a dangerous burst of rapid discharges, and ablationof these foci produced a concomitant dramatic decrease in thetotal number of ectopic beats and short-term recurrences ofatrial fibrillation. In nine patients, isolated ectopic beatswere used as a guide for ablation without mapping the initiationof atrial fibrillation. In some patients, the focus dischargedonly in bursts inducing fibrillation, without producing isolatedectopic beats. The short triggering burst differs from the "focalatrial fibrillation" observed in a few patients in whom a singlefocus fires for sustained periods without leading to typicalintracardiac fibrillation owing to a near-normal substrate.23
The concept that paroxysms of atrial fibrillation are initiatedby discharges from one or only a few focal sources has importantimplications. Repetitive discharges can produce progressivepathologic changes in the atrial substrate that may lead tothe self-perpetuation of atrial fibrillation.33 The focus respondsto curative therapy with minimal catheter ablation, which cansuppress the trigger and may reduce the potential degenerationof the atrial substrate. This approach has the advantage overrate-control therapies of maintaining sinus rhythm, and itsuse may decrease the morbidity associated with other, more extensivecurative procedures.9,10,11,12,13,14,15,16,17,18,19,20,34,35
The successful ablation of foci was safely achieved, and theprocedure eliminated previously frequent atrial fibrillationwithout a need for antiarrhythmic drugs in 84 percent of thepatients during hospital monitoring and in 62 percent afterdischarge. Of note, most of the recurrent atrial fibrillationwas associated with recurrent ectopic beats, indicating thata better technique of mapping or of ablation may further improvethese results. Important limitations inherent in the managementof atrial fibrillation are the difficulty of obtaining reliabledata on arrhythmia and its initiation on an outpatient basisand the uncertain duration of asymptomatic episodes.36 Additionalstudies are necessary to evaluate the role of ablation of triggeringectopic foci in preventing atrial fibrillation, as well as thesafety of ablation in the pulmonary veins, before widespreadapplication of ablation for the treatment of this common cardiac-rhythmdisturbance can be recommended.
Source Information
From the Hôpital Cardiologique du Haut-Lévêque, Ave. de Magellan, 33604 Bordeaux-Pessac, France, where reprint requests should be addressed to Dr. Haïssaguerre.
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