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Europace Advance Access originally published online on June 26, 2007
Europace 2007 9(8):627-632; doi:10.1093/europace/eum124
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© The European Society of Cardiology 2007. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

ATRIAL FIBRILLATION

Exercise testing for non-invasive assessment of atrial electrophysiological properties in patients with persistent atrial fibrillation

Oliver Husser1, Daniela Husser1,2, Martin Stridh3, Leif Sörnmo3, Valentina D.A. Corino4, Luca T. Mainardi4, Federico Lombardi5, Helmut U. Klein1, S. Bertil Olsson2 and Andreas Bollmann1,2,*

1 Department of Cardiology, Otto-von-Guericke University, University Hospital, Leipziger Str. 44, 39120 Magdeburg, Germany; 2 Department of Cardiology, Lund University, Lund, Sweden; 3 Department of Electroscience, Lund University, Lund, Sweden; 4 Dipartimento di Bioingegneria, Politecnico di Milano, Milano, Italy; 5 Cardiologia, Dipartimento di Medicina, Chirurgia e Odontoiatria, Osp. San Paolo, University of Milan, Italy

Manuscript submitted 16 April 2007. Accepted after revision 27 May 2007.

* Corresponding author. Tel: +49 391 67 13203. E-mail address: andreas.bollmann{at}medizin.uni-magdeburg.de


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
Aims Experimental studies suggest that the autonomic nervous system modulates atrial refractoriness and conduction velocity in atrial fibrillation (AF). These modulatory effects are, however, difficult to assess in the clinical setting. This study sought to non-invasively characterize in patients with persistent AF, the influence of autonomic modulation induced by exercise on atrial fibrillatory rate as marker of atrial refractoriness and to identify clinical and electrocardiographic predictors of atrial rate response.

Methods and results In 24 patients (16 males, mean age 60 ± 13 years) with persistent AF (16 ± 25 months), continuous ECGs were recorded during bicycle exercise testing. Fibrillatory rate (in fibrillations per minute, fpm) was assessed at baseline and immediately after termination of exercise with spatiotemporal QRST cancellation and time–frequency analysis. Ventricular response was characterized by time-domain HRV indices. Exercise had no influence on mean fibrillatory rate (409 ± 42 vs. 414 ± 43 fpm, P = NS). Seven patients responded to exercise with an increase in fibrillatory rate (26 ± 10 fpm, P < 0.001 and three with a decrease (–21 ± 8 fpm, P < 0.001), while the remaining 14 patients did not show a response. Responders' HRV indices changed in response to exercise similarly to that of non-responders. Their baseline fibrillatory rate was, however, lower than that of non-responders (387 ± 18 vs. 425 ± 48 fpm, P = 0.028). No other clinical or echocardiographic variable was associated with fibrillatory rate response. Twelve weeks after cardioverson, responders were more likely to remain in sinus rhythm than non-responders (88 vs. 46 %, P = 0.04).

Conclusions Exercise-induced autonomic activation produces changes in atrial electrophysiological properties that can be detected by time–frequency analysis. Higher baseline fibrillatory rates are associated with an impaired atrial response to exercise that suggests advanced electrical remodelling and reduced sensitivity to autonomic stimuli.

Key Words: Atrial fibrillation, Autonomic nervous system, Exercise testing, ECG


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
The autonomic nervous system has modulating effects on atrial electrophysiological properties in patients with atrial fibrillation (AF) and may influence induction and maintenance but also termination of the arrhythmia. Supporting mechanisms behind AF sustenance are that both vagal and sympathetic stimulation reduce atrial refractory periods and increase atrial heterogeneity thus favouring re-entry.1Go

Exercise testing is associated with withdrawal of parasympathetic tone and concomitant increase of sympathetic tone2Go and is commonly used in clinical practice for evaluation of coronary heart disease and/or diagnosis of exercise-induced arrhythmias.3Go Limited information is available on the effects of exercise on atrial electrophysiological properties during AF particularly when they are assessed non-invasively.

Fibrillatory rate has been introduced as a marker for atrial refractoriness and complexity of atrial activation in AF.4Go Several studies made use of fibrillatory rate obtained from the surface ECG in order to monitor electrophysiological properties of the fibrillating atria for analysing antiarrhythmic drug actions or spontaneous diurnal variability.5Go Information on atrial response to exercise is still lacking.

Consequently, the purpose of this study was (i) to non-invasively characterize exercise effects on atrial fibrillatory rate in patients with persistent AF and (ii) to identify clinical and electrocardiographic predictors of fibrillatory rate response.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
Patients
This study included 24 consecutive patients with persistent AF undergoing exercise testing. Clinical characteristics and echocardiographic parameters are presented in Table 1. All patients provided written informed consent before study participation.


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  		Table 1 Clinical and echocardiographic characteristics of the study population

 
All patients underwent symptom-limited bicycle exercise stress testing using a 3-min step-up protocol. Workload increase was chosen according to age- and gender-predicted values, aiming for a test-duration of 8–12 min.

Those 24 patients were the first set of a cardioversion study, whose study protocol has been published previously.6Go In short, after baseline testing, patients received oral flecainide (200–300 mg/day, n = 15) or amiodarone (1200 mg for 7 days, followed by 200 mg/day, n = 9) for 3–5 days and underwent electrical cardioversion if AF persisted. Atrial fibrillation recurrences were determined by ECG and Holter ECG 24 h, 2 and 12 weeks after cardioversion or when patients' symptoms suggested AF.

As with previous investigations,7Go,8Go for the purpose of this study early AF recurrence was defined as relapse into AF within 2 weeks following successful cardioversion. Since fibrillatory rate reflects atrial refractory periods and their normalization has been found to occur within days to weeks following cardioversion,9Go this follow-up interval was also chosen from a pathophysiological background.

ECG acquisition and analysis
A continuous 3-lead ECG (Predictor, Dr Kaiser; 2000 Hz sampling rate) was recorded with the subject in a supine position before class I or III antiarrhythmic drug initiation. Fibrillatory rate was assessed in 2-min ECG segments at rest and immediately after termination of exercise with spatiotemporal QRST cancellation and time–frequency analysis.

Time–frequency analysis10Go was performed on a bipolar lead whose electrodes were positioned below the left clavicle and at the right sternal border at the sixth intercostal space.11Go

In short, QRST complexes were subtracted using spatiotemporal QRST cancellation12Go and the resulting fibrillatory signal was downsampled to 50 Hz and subjected to spectral analysis. The time–frequency distribution of the atrial signal, which was obtained by short-term Fourier transform, was decomposed such that each spectrum could be modelled as a frequency shifted and amplitude-scaled version of the spectral profile. This procedure is based on a spectral profile, dynamically updated from previous spectra, which is matched to each new spectrum using weighted least squares estimation. The frequency shift needed to achieve optimal matching then yields a measure of instantaneous fibrillatory rate of a 2.5-s electrocardiographic segment (overlapping with one segment each second) and is trended as a function of time (Figure 1). Mean fibrillatory frequency was converted to fibrillatory rate (rate = frequency x 60) and expressed in fibrillations per minute (fpm).


Figure 1
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  		Figure 1 Time–frequency analysis of AF. Two seconds (out of a 1-min recording) of an ECG signal from a patient with AF (upper panel), and the same interval after spatiotemporal QRST cancellation (middle panel, amplitude scale is magnified five times). This fibrillatory signal is then subjected to spectral analysis techniques. Time–frequency distribution (left box), power frequency spectrum (middle box), and frequency trend (right box).

 
It should be noted that the time–frequency analysis includes techniques for rejecting segments with poor signal quality.13Go Thus, the mean fibrillatory rate is computed from segments with reliable rate estimates only, as opposed to conventional power spectral analysis where all segments are included.

An atrial rate response to exercise was considered present if atrial rate changed by > ± 2.5%. This definition is based on previous observations that there is a ≤ 2.5% natural variation of fibrillatory rate in 1-min recordings under stationary conditions.14Go–16Go

As previously reported for AF analysis,17Go ventricular response was characterized by mean NN (mean of normal-to-normal RR intervals), SDNN (standard deviation of normal-to-normal RR intervals), rMSSD (root-mean-square of successive NN differences), and pNN50 (percentage of NN intervals >50 ms different from preceding interval).

Statistical analysis
Continuous variables are presented as mean ± one standard deviation. Atrial and ventricular rate responses to exercise were assessed using Student's t-test for paired data. Atrial rate and ventricular response parameters were correlated using Pearson correlation. Responders and non-responders were compared using Student's t-test for unpaired data for continuous and {chi}2 test for categorical variables. Multivariate analysis was applied to identify independent predictors of fibrillatory rate response including variables with a P-value < 0.15 found in univariate analysis. The relation between fibrillatory rate as well as its exercise response and AF recurrences was also analysed using Student's t-test for unpaired data and {chi}2 test. A P-value < 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusions
 Acknowledgements
 References
 
Exercise effects on ECG parameters
Exercise resulted in reduction in mean NN, SDNN, rMSSD, and pNN50 (Table 2), but had no influence on mean fibrillatory rate (409 ± 42 vs. 414 ± 43 fpm, P = NS). There was no correlation between fibrillatory rate and ventricular rate parameters at rest or after exercise.


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  		Table 2 Exercise-induced changes in ventricular response

 
Looking at individual fibrillatory rate responses, 14 patients did not show a rate change > ± 2.5%. However, 10 patients responded to exercise with either an increase in fibrillatory rate (n = 7, 26 ± 10 fpm or 6.8 ± 2.6%, P < 0.001) or a decrease (n = 3, –21 ± 8 fpm or –5.5 ± 2.0%, P < 0.001).

Responders' clinical and ventricular response variables as well as exercise duration and intensity were comparable with that of non-responders (Table 3). However, responders had a lower baseline fibrillatory rate than their counterparts with no atrial rate response (387 ± 18 vs. 425 ± 48 fpm, P = 0.028) in uni- (Table 3) and multivariate analysis (ß = –0.034, P = 0.04).


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  		Table 3 Clinical and ECG variables in responders and non-responders

 
As shown in Figure 2, a baseline cut-off rate of 395 fpm predicted a fibrillatory rate response to exercise with a sensitivity of 70% and a specificity of 79% (AUC = 0.743). None of the patients with a baseline fibrillatory rate > 420 fpm responded to exercise with fibrillatory rate changes.


Figure 2
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  		Figure 2 Relation between baseline fibrillatory rate and response to exercise. Best predictive accuracy was obtained with a cut-off of 395 fpm (thick line). Please note that none of the patients with a baseline fibrillatory rate > 420 fpm responded to exercise with fibrillatory rate changes (dashed line).

 
Exercise effects and AF recurrence
During the follow-up period after cardioversion, there were eight AF recurrences (all at 2 weeks), while sinus rhythm was observed in 14 patients. In one patient cardioversion failed, and in one patient atrial flutter developed; both were excluded from this sub-analysis.

Baseline fibrillatory rate was similar in patients still in sinus rhythm compared with patients with AF recurrence (408 ± 41 vs. 422 ± 45 fpm, P = NS). However, exercise responders were more likely to remain in sinus rhythm than non-responders (88 vs. 46%, P = .04). Clinical characteristics and ventricular rate parameters were not associated with AF recurrence.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusions
 Acknowledgements
 References
 
This study shows, for the first time, that exercise-induced adrenergic activation and reduced parasympathetic modulation may produce contrasting effects on atrial electrophysiological properties which resulted in an increase (n = 7) or decrease (n = 3) in fibrillatory rate or no change at all (n = 14). No changes were detectable in patients with higher baseline fibrillatory rates in spite of a preserved exercise-induced ventricular response. Preliminary data suggest that atrial rate response to exercise may be predictive of AF recurrences after sinus rhythm restoration.

The role of the autonomic nervous system in AF
The autonomic nervous system modulates atrial electrophysiological properties in patients with AF. To a greater extent than the ventricles, both parasympathetic and sympathetic nerves richly innervate the atria. Autonomic activation at the atrial level produces complex effects: for example, in animal experiments, atrial effective refractory period is shortened favouring re-entry during both sympathetic and vagal stimulation18Go,19Go although the changes induced by parasympathetic stimulation are of greater magnitude.18Go Atrial automaticity is instead significantly augmented by adrenergic stimulation.20Go Some recent data in humans suggest that chronic fibrillating atria are more under sympathetic than vagal control21Go and the higher incidence of AF in states characterized by adrenergic activation such as progressing heart failure22Go,23Go supports the hypothesis that the sympathetic nervous system plays an important role in the maintenance of this arrhythmia.

Nevertheless, the final effects of autonomic modulation are difficult to assess in the clinical setting taking into account the number of factors that may affect the autonomic profile in each patient and the possibility that atria and ventricles may differently respond to autonomic stimulation.

Comparison with previous studies
Since atrial rates obtained from the surface ECG closely reflect intra-atrial rates10Go,16Go,24Go and are a marker of atrial refractoriness,25Go atrial fibrillatory rate seems to be ideal for monitoring the effects of autonomic tone changes which occur spontaneously during a 24-h period or by specific interventions that may activate the autonomic nervous system. Indeed, the circadian variability of atrial fibrillatory rate has been previously explored,14Go,26Go and the response to carotid sinus massage15Go or head-up tilt testing21Go reported. Common findings were an increase in fibrillatory rates in conditions characterized by a sympathetic stimulation/vagal withdrawal as during daytime or with head-up tilting.

Our results are partially in agreement with the earlier findings. Indeed, some of our patients, responded to exercise with a fibrillatory rate increase, while in contrast, a reduction of fibrillatory rate during exercise was observed in others. Considering the latter, it may be worth recalling that contrasting results have also been reported in previous studies on the circadian fibrillatory rate behaviour in patients with persistent AF.14Go It has been found that fibrillatory rate decreased concomitantly with an increase in ventricular rate in the morning hours when sympathetic control mechanisms are prevailing. The existence of this control mechanism is supported by the clinical observation that in some patients AF can also be self-terminated by exercise.27Go In these cases, a fibrillatory rate decrease prior to AF termination may occur, as it has been reported for drug-induced termination.24Go

In all patients of our series, the different responses of fibrillatory rates occurred during a withdrawal of parasympathetic tone and concomitant increase of sympathetic tone as evidenced by changes in NN, SDNN, rMSSD, and pNN50 (despite different cardiac pathologies and medications).2Go,17Go It may be speculated that depending on the dominance of one limb of the autonomic nervous system over the other in supporting AF sustenance in the individual patient, fibrillatory rate increased with further sympathetic stimulation if the sympathetic limb is dominant or decreased with vagal withdrawal if the parasympathetic limb is dominant.

To understand why the majority of our patients did, however, not respond to exercise with fibrillatory rate changes, the observation that a high baseline fibrillatory rate was the only predictor for this behaviour is of interest. This could be interpreted as indirect evidence that electrical remodelling indicated by a faster rate, is associated to a decreased sensitivity to autonomic modulation. This possibility is also supported by the results of a previous study showing that AF patients with a higher fibrillatory rate displayed a lesser degree of circadian atrial rate variability.26Go

Of special note is also the different behaviour of atrial and ventricular rate responses and the poor correlation between changes in atrial fibrillatory rate and ventricular response. In fact, although there was a rather homogeneous ventricular response, the response of atrial activity was—as discussed in detail before—highly variable thus conforming the different effects of autonomic control mechanisms at the atrial and atrio-ventricular node levels. At this regard, these data also indicate that atrial fibrillatory activity (concealed conduction) is a less important determinant of ventricular rate response during AF than atrio-ventricular conduction properties.28Go

Although not the main purpose, this study extends previous observations on the relation between electrical remodelling, autonomic activity, and early AF recurrences. This study revealed that subjects who responded to exercise with fibrillatory rate changes had a higher chance to remain in sinus rhythm, while non-responders had a high risk for AF recurrence. On the one hand, a low baseline fibrillatory rate has been suggested as marker of less electrical remodelling which was associated with lower risk for AF recurrences.6Go On the other hand, an abnormal autonomic control has also been suggested to contribute to electrical remodelling and consequently to a higher risk for AF recurrences.8Go

Limitations
This study is limited by its sample size including a heterogeneous patient population with different cardiac pathologies and medications. Nevertheless, in agreement with experimental and clinical studies, different types of rate responses to exercise could be identified. Interestingly, they were associated with baseline fibrillatory rate and cardioversion outcome but not with other clinical variables. Of special note, underlying heart disease, AF duration, or cardioactive medication did not effect fibrillatory rate responses to exercise in uni- and multivariate analysis but the sample size may have prohibited its detection.

Although the net effects of exercise on sympathetic stimulation, and/or vagal withdrawal cannot be quantified in the individual patient, importantly, ventricular responses were consistent among all individuals indicating a comparable autonomic stimulus.

Finally, spatio-temporal QRST cancellation and time–frequency analysis were performed at baseline and immediately after exercise termination (not during exercise) due to substantial exercise-induced moving artefact and noise.


   Conclusions
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
Acknowledgements
 References
 
Exercise-induced changes in the autonomic nervous system modulate atrial electrophysiological properties, which can be analysed by means of time–frequency analysis. Patients with faster fibrillatory rates at rest and consequently no rate response to exercise are characterized by a higher degree of electrical remodelling which is associated with a reduced sensitivity to autonomic modulation and possibly greater risk for early AF recurrences.

Thus, exercise testing may add valuable information on the autonomic and electrophysiological status of the atria in the individual patient with AF.


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
References
 
This study has been performed in and supported in part by the NordForsk network ‘Electrocardiology in Atrial Fibrillation’. D.H. and M.S. are supported by the Volkswagen Foundation, Germany.

Conflict of interest: none declared.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
[1] Chen J, Wasmund SL, Hamdan MH. Back to the future: the role of the autonomic nervous system in atrial fibrillation. Pacing Clin Electrophysiol (2006) 29:413–21.[CrossRef][Medline]

[2] Task Force of the European Society of Cardiology:the North American Society of Pacing:Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation (1996) 93:1043–65.[Free Full Text]

[3] Gibbons RJ, Balady GJ, Bricker JT, Chaitman BR, Fletcher GF, Froelicher VF, et al. ACC/AHA 2002 guideline update for exercise testing: summary article: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Update the 1997 Exercise Testing Guidelines). Circulation (2002) 106:1883–92.[Free Full Text]

[4] Konings KT, Kirchhof CJ, Smeets JR, Wellens HJ, Penn OC, Allessie MA. High-density mapping of electrically induced atrial fibrillation in humans. Circulation (1994) 89:1665–80.[Abstract/Free Full Text]

[5] Bollmann A, Husser D, Mainardi L, Lombardi F, Langley P, Murray A, et al. Analysis of surface electrocardiograms in atrial fibrillation: techniques, research, and clinical applications. Europace (2006) 8:911–26.[Abstract/Free Full Text]

[6] Bollmann A, Husser D, Steinert R, Stridh M, Sörnmo L, Olsson SB, et al. Echo- and electrocardiographic predictors for atrial fibrillation recurrence following cardioversion. J Cardiovasc Electrophysiol (2003) 14:S162–65.[CrossRef][Web of Science][Medline]

[7] Tieleman RG, Van Gelder IC, Crijns HJ, De Kam PJ, Van Den Berg MP, Haaksma J, et al. Early recurrences of atrial fibrillation after electrical cardioversion: a result of fibrillation-induced electrical remodeling of the atria? J Am Coll Cardiol (1998) 31:167–73.[Abstract/Free Full Text]

[8] Lombardi F, Colombo A, Basilico B, Ravaglia R, Garbin M, Vergani D, et al. Heart rate variability and early recurrence of atrial fibrillation after electrical cardioversion. J Am Coll Cardiol (2001) 37:157–62.[Abstract/Free Full Text]

[9] Yu WC, Lee SH, Tai CT, Tsai CF, Hsieh MH, Chen CC, et al. Reversal of atrial electrical remodeling following cardioversion of long-standing atrial fibrillation in man. Cardiovasc Res (1999) 42:470–6.[Abstract/Free Full Text]

[10] Husser D, Stridh M, Cannom DS, Bhandari AK, Girsky MJ, Kang S, et al. Validation and clinical application of time-frequency analysis of atrial fibrillation electrocardiograms. J Cardiovasc Electrophysiol (2007) 18:41–6.[CrossRef][Web of Science][Medline]

[11] Waktare JE, Gallagher MM, Murtagh AM, Camm AJ, Malik M. Optimum lead positioning for recording bipolar atrial electrocardiograms during sinus rhythm and atrial fibrillation. Clin Cardiol (1998) 21:825–30.[Web of Science][Medline]

[12] Stridh M, Sörnmo L. Spatiotemporal QRST cancellation techniques for analysis of atrial fibrillation. IEEE Trans Biomed Eng (2001) 48:105–11.[CrossRef][Web of Science][Medline]

[13] Stridh M, Bollmann A, Olsson SB, Sörnmo L. Time-frequency analysis of atrial tachyarrhythmias: detection and feature extraction. IEEE Eng Med Biol Mag (2006) 25:31–9.[CrossRef][Web of Science][Medline]

[14] Bollmann A, Sonne K, Esperer HD, Toepffer I, Klein HU. Circadian variations in atrial fibrillatory frequency in persistent human atrial fibrillation. Pacing Clin Electrophysiol (2000) 23:1867–71.[Medline]

[15] Bollmann A, Wodarz K, Esperer HD, Toepffer I, Klein HU. Response of atrial fibrillatory activity to carotid sinus massage in patients with atrial fibrillation. Pacing Clin Electrophysiol (2001) 24:1363–8.[CrossRef][Medline]

[16] Holm M, Pehrson S, Ingemansson M, Sörnmo L, Jahansson R, Sandhall L, et al. Non-invasive assessment of the atrial cycle length during atrial fibrillation in man: introducing, validating and illustrating a new ECG method. Cardiovasc Res (1998) 38:69–81.[Abstract/Free Full Text]

[17] van den Berg MP, Haaksma J, Brouwer J, Tieleman RG, Mulder G, Crijns HJ. Heart rate variability in patients with atrial fibrillation is related to vagal tone. Circulation (1997) 96:1209–16.[Abstract/Free Full Text]

[18] Liu L, Nattel S. Differing sympathetic and vagal effects on atrial fibrillation in dogs: role of refractoriness heterogeneity. Am J Physiol (1997) 273:H805–16.[Web of Science][Medline]

[19] Takei M, Furukawa Y, Narita M, Ren LM, Karasawa Y, Murakami M, et al. Synergistic nonuniform shortening of atrial refractory period induced by autonomic stimulation. Am J Physiol (1991) 261:H1988–93.[Web of Science][Medline]

[20] Coumel P. Autonomic influences in atrial tachyarrhythmias. J Cardiovasc Electrophysiol (1996) 7:999–1007.[Web of Science][Medline]

[21] Ingemansson MP, Holm M, Olsson SB. Autonomic modulation of the atrial cycle length by the head up tilt test: non-invasive evaluation in patients with chronic atrial fibrillation. Heart (1998) 80:71–6.[Abstract/Free Full Text]

[22] The CONSENSUS Trial Study Group. Effects of enalapril on mortality in severe congestive heart failure. Results of the Cooperative North Scandinavian Enalapril Survival Study (CONSENSUS). N Engl J Med (1987) 316:1429–35.[Abstract]

[23] The SOLVD Investigators. Effect of enalapril on mortality and the development of heart failure in asymptomatic patients with reduced left ventricular ejection fractions. N Engl J Med (1992) 327:685–91.[Abstract]

[24] Bollmann A, Kanuru NK, McTeague KK, Walter PF, DeLurgio DB, Langberg JJ. Frequency analysis of human atrial fibrillation using the surface electrocardiogram and its response to ibutilide. Am J Cardiol (1998) 81:1439–45.[CrossRef][Web of Science][Medline]

[25] Capucci A, Biffi M, Boriani G, Ravelli F, Nollo G, Sabbatani P, et al. Dynamic electrophysiological behavior of human atria during paroxysmal atrial fibrillation. Circulation (1995) 92:1193–202.[Abstract/Free Full Text]

[26] Meurling CJ, Waktare JE, Holmqvist F, Hedman A, Camm AJ, Olsson SB, et al. Diurnal variations of the dominant cycle length of chronic atrial fibrillation. Am J Physiol Heart Circ Physiol (2001) 280:H401–6.[Abstract/Free Full Text]

[27] Ragozzino MW, Snyder J, Nayak HM. Self-cardioversion of paroxysmal lone atrial fibrillation with exercise. N Engl J Med (2002) 347:2085–6.[Free Full Text]

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