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Europace Advance Access published online on July 13, 2007
Europace, doi:10.1093/europace/eum108
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© The European Society of Cardiology 2007. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Difference between electrical remodelling after pulmonary veins and right atrium appendage pacing

Kebbati A. Hafid, Huang Cong Xin*, Wang Xi, Zhao Qing Yan and Yang Bo

Department of Cardiology, Renmin Hospital of Wuhan University, Jiefang Road 238, Wuhan 430060, People's Republic of China

Manuscript submitted 13 November 2006. Accepted after revision 26 April 2007.

* Corresponding author. Tel: +86 276 295 9239; fax: +86 27 88040334. E-mail address: huangcongxin{at}yahoo.com.cn


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Limitations of the study
 Acknowledgements
 References
 
Objective Pulmonary veins (PVs) are important sources of paroxysmal atrial fibrillation (AF). Rapid atrial pacing changes atrial electrophysiology, and facilitates the induction and maintenance of AF. The purpose of our study was to evaluate the changes in atrial effective refractory period (AERP) proprieties and in ionic currents in PVs myocytes from dogs subjected to rapid atrial pacing in PVs and right atrial appendage (RAA) and to relate these changes to the ability to induce AF.

Methods Twelve mongrel dogs in normal sinus rhythm were paced from the superior left PVs or RAA at 500 bpm for 4 h. Electrophysiological studies were conducted to determine the changes in AERP, dispersion, and rhythm. Ionic currents were evaluated using patch clamp technique in single PVs myocytes in sham-operated dogs, and the results were compared with those from PVs and RAA pacing groups.

Results The presence of rapid atrial pacing was associated with a marked shortening in AERP in both PVs and RAA pacing group with a marked increase in AERP dispersion in PVs pacing. Both L-type calcium current (ICa,L) and the transient outward current (Ito) were reduced in both groups with an increased significance in PVs pacing group. The density of ICa,L was decreased significantly from (–6.03 ± 0.63) pA/pF in the control group to (–3.21 ± 0.34) pA/pF in the PVs pacing group and (–4.75 ± 0.41) pA/pF in the RAA pacing group (n = 6, P < 0.05), whereas the density of Ito was decreased significantly from (8.45 ± 0.71) pA/pF in the control group to (5.21 ± 0.763) pA/pF in the PVs pacing group and (6.84 ± 0.69) pA/pF in the RAA pacing group (n = 6, P < 0.05).

Conclusion Our findings provide likely ionic mechanisms of shortened repolarization in induced atrial tachycardia with a decrease in ICa,L and Ito densities, which is the likely mechanism for a decrease in action potential duration rate adaptation in the canine rapid pacing model more pronounced in the PVs pacing group underlying the crucial role of PVs in initiating AF.

Key Words: Pulmonary vein, Atrial fibrillation, Ca2+ channel, K+ channel, Remodeling, Canine


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Limitations of the study
 Acknowledgements
 References
 
Atrial fibrillation (AF) is the most common arrhythmia in humans. In recent years, the functional mechanisms underlying AF have been investigated in animal models1Go,2Go and in human.3Go,4Go From these studies, it became evident that AF is characterized by a marked decrease in the atrial effective refractory period (AERP), AERP adaptation to rate,1Go,4Go as well as atrial conduction velocity;3Go thereby favouring the occurrence of multiple wavelet re-entry. Changes in the AERP are generally assumed to reflect atrial electrical remodelling,5Go occurring as an accompaniment of AF and/or consequent to rapid atrial pacing or atrial tachyarrhythmias.1Go,2Go The spatial heterogeneity of AERP appears to be an important determinant of the ability of AF to maintain itself.6Go,7Go Recent studies suggest that changes in the AERP caused by sustained atrial tachycardia are spatially variable, both among and within different atrial regions, resulting in an increased ERP heterogeneity that contributes importantly to the AF-promoting effects of atrial remodelling.7Go In many instances, an important factor in the initiation of AF is the presence of ectopic foci in the pulmonary veins (PVs).8Go Atrial ectopy, whether spontaneous, as with pulmonary venous foci, or paced, often is a cause of altered atrial activation. Spatial difference in the AERP plays an important role in the initiation and perpetuation of atrial re-entrant arrhythmias.9Go Regional differences in AERP have been attributed to differences in ionic currents and action potential duration (APD).10Go In isolated canine atria, Spach et al.11Go,12Go found an inverse relationship between atrial APD or AERP and distance from the sinus node. Whether this spatial distribution between APD and AERP is a long-term result of the sequence of activation during sinus rhythm (SR) or intrinsic electrophysiological differences between atrial myocytes in different parts of the atria is unclear. Although much is known about these functional mechanisms of AF, the nature of cellular abnormalities and, in particular, changes in ionic currents that promote AF have not yet been completely determined; therefore, the purpose of the present study is to evaluate different changes in AERP properties and in ionic currents in PVs myocytes from dogs subjected to rapid pacing in left superior PVs and right atrial appendage (RAA) and to relate these different changes to the ability to induce AF.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Limitations of the study
 Acknowledgements
 References
 
Preparation of the canine model
Twelve normal mongrel dogs weighing 12–25 kg (mean, 18.4 ± 4.7 kg) were used in this study. The study protocol was approved by the Ethics Committee of Wuhan University Medical College, and animal handling was carried out according to the Wuhan Directive for Animal Research. The dogs were anaesthetized with intraperitoneal (i.p.) injection of sodium pentobarbital (30 mg/kg, additional doses of 4 mg/kg as needed). The surface ECG was continuously monitored. The animals were intubated and ventilated with a positive pressure ventilator. A median sternotomy was performed using sterile technique. In the PVs pacing group, the electrodes for pacing were attached in the left superior pulmonary vein and the recording leads were attached in the superior left PVs, RAA, left atrial appendage (LAA), right atrium (RA), and left atrium (LA), whereas in the RAA pacing group, the electrodes for pacing were attached in the RAA and the recording leads were attached in superior left PVs, RAA, LAA, RA, and LA. All the 12 dogs were paced to a rate of 500 bpm. Pacing was maintained for 4 h. The heart was removed immediately after the predetermined durations of stimulation. ICa,L and Ito were recorded using the whole-cell patch clamp technique.

Electrophysiological measurements
Electrophysiological studies were performed during SR and 1 2, 3, and 4 h after each pacing drive. AERP was determined using a LEAD-2000B instrument (Sichuan, People's Republic of China). The refractory period was determined at five atrial regions: RAA, LAA, RA, LA, and PVs. AERP were measured by single premature stimuli (2 ms, twice threshold). An extrastimulus (S2) was interpolated at every eight interval during PVs pacing (S1–S1 250 ms). Starting well within the refractory period, the A1–S2 coupling interval was increased in 2-ms steps. The shortest coupling interval resulting in a propagated response was considered AERP. Spatial dispersion in refractory periods was defined as the difference between the longest and shortest refractory of the fifth regional AERPs.

Cell isolation and patch clamp technique
Immediately after cardiac excision, the hearts was immersed in normal sodium at 0°C. The tissue of PVs was dissected and quickly transferred to Ca2+-free Tyrode solution (30 mL) containing (mM): 136 NaCl, 5.4 KCl, 1 MgCl2, 0.33 NaH2PO4, 10 glucose, and 5 HEPES (pH 7.4) with 100% O2 at 37°C. Tissues were cut about 1 mm3Go and washed three times with tyrode solution (5 min/wash). Then, CLS II Collagenase and 0.1% bovine serum albumin was added to the preparation. At the same time, 30 mL CaCl2 (5 mM) was added to the preparation for four times (10 min/every time). After ~45 min, only quiescent and rod-shaped cells with clear cross striation were selected. Those cells were perfused with the Tyrode solution containing: 136 NaCl, 5.4 KCl, 1 CaCl2, 1 MgCl2, 10 glucose, and 5 HEPES (pH 7.4). The ionic currents were recorded using whole cell configuration of the voltage clamp technique, using an EPC-9 amplifier (HEKA Instruments, Germany). Borosilicate glass electrodes (outer diameter 1.0 mm), connected to the patch clamp amplifier, with resistance of ~1 M{Omega} were used to record INa and 3–5 M{Omega} were used for recording of action potentials and others ionic currents. Data were sampled with an A/D converter (Digidata 1200, Axon Instruments, USA) and stored for subsequent analysis. The pipette solution for ICa,L measurement contained (mM): 120 CsCl, 1 CaCl2, 5 MgCl2, 11 EGTA, 10 HEPES, 5 Na2ATP, and 11 glucose, whereas the pipette solution for Ito measurement contained (mM): 45 KCl, 5 Mg ATP, 10 EGTA, 10 HEPES, 11 glucose, 85 K-aspartate, and 5 N-pyruvate. The bath solution contained (mM): 136 NaCl, 5.4 KCl, 1 CaCl2, 1 MgCl2, 10 glucose, and 10 HEPES.

Statistical analysis
Values are shown as the mean ± SEM, and SPSS statistical software was used. Statistical comparison was made using ANOVA. Paired and unpaired comparisons were conducted using the Student's t-test. Coefficient of variance (CV) was calculated to assess the precision of our technique. Results were considered significant with P-values <0.05.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Limitations of the study
 Acknowledgements
 References
 
Sinus rhythm
AERP was longest at RAA and LAA, and was significantly shorter at PVs. Difference between RA and LA refractory periods were not statistically significant. Table 1 lists the AERP values from five atrial sites.


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  		Table 1 Atrial effective refractory period (AERP) during sinus rhythm and each hour during PVs and RAA pacing

 
PVs pacing and RAA pacing
The increase in atrial rate, from 200 ± 5 bpm during normal SR to 500 bpm during PVs and RAA pacing, was associated with AERP shortening that appears quickly, and was progressive and persistent with an increased dispersion in AERP (Table 1). The mean rate of capture was 315 ± 4 bpm in the PV pacing group against 312 ± 3 bpm in the RAA pacing group. The shorter AERP after 4 h pacing was measured in PVs site during PVs pacing and RAA pacing with a value of 113 ± 9 ms in the PVs pacing group against 122 ± 9 ms in the RAA pacing group. The dispersion of AERP was statistically significant in the PVs pacing group after 4 h pacing with a value of 23 ± 4.3 ms (Figure 1). In both PV and RAA pacing groups, CV tends to increase over pacing time. In PV site, the CV was 5% in both groups before pacing, and increased to 8 and 7.3% in PV and RAA pacing groups, respectively.


Figure 1
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  		Figure 1 Spatial distribution of atrial refractory periods during sinus rhythm.

 
Atrial fibrillation
All animals were tested for AF inducibility. No spontaneous atrial arrhythmias were detected before or during atrial pacing. Three of six dogs during PVs pacing and one of six dogs during RAA pacing developed AF. The time course of AF was 15, 22, and 17 s, respectively, in the PVs pacing group and 11 s in the RAA group. The mean AF cycle length is represented in Table 2. However, because of the relatively small animal group (n = 6) and the high inter-individual variation, the difference was not statistically significant.


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  		Table 2 Mean atrial fibrillation cycle length in pulmonary veins and right atrial appendage site

 
Effects of rapid pacing on potassium current
Currents were recorded under conditions designed to eliminate INa and ICa. Ito was measured in six SR, six PVs pacing, and six RAA pacing cells.

Figure 2 shows representative recordings of steady-state currents from a cell of an SR group (Figure 2A), a cell from PVs pacing group (Figure 2B) and a cell from RAA pacing group (Figure 2C). The current–voltage (I–V) relations for Ito in the three groups are illustrated in Figure 2D. Ito densities were significantly reduced at all test potentials positive to 0 mV, i.e. at +70 mV, 8.45 ± 0.71 pA/pF in SR to 5.21 ± 0.73 pA/pF in the PVs pacing group and to 6.84 ± 0.69 pA/pF in the RAA pacing group. In the PVs pacing group, the presence of pacing was associated with a significant decrease in Ito value; in RAA pacing group also the Ito value decreased, but did not reach the statistical significance level. In SR, a large, transient, rapidly inactivating Ito was visible, which was almost absent in pacing groups.


Figure 2
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  		Figure 2 (A)–(C) Recordings of Ito obtained with the voltage protocol shown in the inset at 0.2 Hz in representative cells obtained from a sham-operated dog (A), dogs subjected to PVs pacing (B) and dogs subjected to RAA pacing. The cardiac cells were held at a holding potential of –80 mV, depolarized to –40 mV for 25 ms to inactivate sodium currents, and then depolarized in 10 mV increments over 500 ms to a test potential of +70 mV. Ito was measured as the difference between the peak amplitude and the current remaining at the end of the pulse. This outward current activated rapidly, inactivated transiently, and then reached steady levels. Ito was activated at –30 mV, the current density increase with the increase in test potential, the peak was reached at +70 mV. The density of Ito was decreased significantly from (8.45 ± 0.71) pA/pF in the control group to (5.21 ± 0.763) pA/pF in PVs pacing group and (6.84 ± 0.69) pA/pF in RAA pacing group (n = 6, P < 0.05). (D) Ito density–voltage relationships of the currents.

 
Effect of rapid pacing in L-type calcium current
ICa,L was studied 5 min after cell membrane rupture in all cells to avoid contaminating effects of ICa,L rundown. Figure 3 shows a typical example of calcium current recorded from a cell of an SR (Figure 3A), a PV pacing (Figure 3B), and an RAA pacing (Figure 3C) groups. Figure 3D shows the I–V relation for six cells in the SR, six cells in the PVs pacing, and six cells in the RAA pacing groups. Induced tachycardia was associated with a marked decrease in ICa,L amplitude in both of pacing groups. The PVs pacing group had a highly significant decrease in ICa,L densities, for example at a test potential of 0 mV, current densities were –6.03 ± 0.63 pA/pF in SR and –3.21 ± 0.34 pA/pF in the PVs pacing group against –4.75 ± 0.41 pA/pF in the RAA pacing group.


Figure 3
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  		Figure 3 (A)–(C) Recordings of ICa,L obtained with the voltage protocol shown in the inset at 0.1 Hz in representative cells obtained from a sham-operated dog (A), dogs subjected to PVs pacing (B), and dogs subjected to RAA pacing. ICa,L was elicited from a holding potential of –50 mV, with 200 ms pulses, increasing from –50 to +50 mV in 10 mV steps. The inactivation was at –60 mV, with 1000 ms, increasing from –56 to +10 mV in 10 mV steps. To avoid the ‘run-down’ effects, ICa,L was measured between 5 and 15 min after rupturing the membrane patch in each cardiomyocyte from the control and pacing groups. When the testing potential was depolarized at +10 mV, ICa,L reached its peak. The density of ICa,L was decreased significantly from (–6.03 ± 0.63) pA/pF in the control group to (–3.21 ± 0.34) pA/pF in the PVs pacing group and (–4.75 ± 0.41) pA/pF in the RAA pacing group (n = 6, P < 0.05). (D) ICa,L density–voltage relationships of the currents.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Limitations of the study
 Acknowledgements
 References
 
Incidence of AF and its relationship to electrophysiological remodelling
In the present study at a pacing rate of 500 bpm, AF occurred in 33% of animals. Atrial electrophysiological remodelling was most readily induced by PVs pacing at rapid rates. Morillo et al.2Go found that following onset of rapid pacing, a short AERP was an important predictor of ease of AF inducibility. Garry13Go showed that electrical stimulation of the atrium of a dog initiated AF. However, the rhythm persisted when the site of stimulation was isolated from the rest of atrium. His observation suggests that although unifocal activity may be important in the initiation of AF, it is not required for its maintenance.

Spatial distribution of atrial refractoriness
In the present study, the longest AERP was found in the RA and LA, whereas AERP in PVs was shorter than in RAA. The shorter refractory period in the PVs is suggested to contribute to the preferential role of the PVs in AF perpetuation. Our findings were similar to these of Chen et al.,14Go they measured the AERP at 16 atrial sites in a control group and in patients with paroxysmal AF. AERP was longest in the Bachmann bundle. The shortest refractory periods were found distal in the PVs and in the inferior RA. Considerable spatial variation in AERP was observed in each atrium, with no overall difference between RA and LA refractoriness. Spach et al.11Go,12Go mapped the local refractory periods in isolated canine RA. The longest refractory periods were found close to the sinus node. The refractory period became shorter at increasing distances from the sinus node. Li et al.10Go showed that the longest AERP was again found at the Bachmann bundle,15Go whereas AERP in the LA wall reportedly was shorter than that in the RA. Li et al.10Go and Oral et al.16Go concluded that the difference may participate in the ability of the LA to act as a ‘driver region’ for AF.

A recent study demonstrated heterogeneity and anisotropid conduction within the PV and at the PV-LA junction in patients undergoing catheter ablation for paroxysmal AF.17Go AF was initiated by re-entry between the distal PV and PV-LA junction or unstable re-entry inside the PV, supporting our hypothesis that re-entrant PV tachycardia is a potential mechanism initiating AF. The crucial role of PV tachycardias in AF was further demonstrated by other investigators,16Go,18Go showing that the immediate recurrence of AF can be caused by PV tachycardias and that short bursts of PV tachycardias are critical in maintaining AF.

Underlying cellular mechanism of the electrophysiological remodelling
In our study, we observed a significant decrease in AERP after rapid pacing. These findings are consistent with previous reports about a shortening in atrial repolarization in vivo. In a goat model, Wijfells et al.1Go demonstrated that AF was associated with a shortening of the AERP and a decrease in ERP adaptation to rate. These findings were confirmed in three studies in the canine rapid atrial pacing model of AF.2Go,19Go,20Go In this model, Yue et al.21Go have also recorded AP, where they found a progressive shortening of the APD and a decrease in APD adaptation to rate with an increased duration of rapid pacing. Zhang et al.4Go studied the effect of chronic AF on AERP and AP in multicellular preparations of human atria. AF was associated with a marked shortening of the AERP and AP, as well as an increased dispersion of repolarization.

In our canine rapid atrial pacing model, the examination of ionic current changes in atrial myocytes from control dogs and dogs subjected to rapid atrial pacing showed an important alteration of ICa,L and Ito, which followed the same time course as the shortening of AERP. Our results emphasize that electrical remodelling might be caused by a reduction in the ICa,L and Ito values, more pronounced in the PVs pacing group explaining the major role of PVs as a sources of paroxysmal AF. PVs myocardial cells develop marked heterogeneity in repolarization, which might cause changes in atrial electrophysiology and facilitates the initiation and maintenance of AF in response to rapid pacing.


   Limitations of the study
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Limitations of the study
Acknowledgements
 References
 
Methods to directly measure atrial refractoriness during AF have recently been developed in animal models, but have yet to be applied to humans. The changes in ionic currents are complex and influenced by many factors. In this study, the short-term effects on Ito and ICa,L were measured. It is very difficult to put these changes in a perspective of changes in the refractory periods or even the ability to induce AF. The current model is based on abrupt changes in AERP and may not reflect the clinical setting.

This study did neither address the question of time course necessary to restore the baseline conditions of AERP nor the ionic changes in atrial myocytes. Further studies are required to address the issue of the role of intra-regional dispersion of atrial refractoriness in the induction and recurrence of clinical AF.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Limitations of the study
 Acknowledgements
References
 
The project was sponsored by the National Natural Science Foundation of China (no. 30470704).

Conflict of interest: none declared.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Limitations of the study
 Acknowledgements
 References
 
[1] Wijffels MCEF, Kirchhof CJHJ, Dorland R, Allessie MA. Atrial fibrillation begets atrial fibrillation: a study in awake, chronically instrumented goats. Circulation (1995) 92:1954–68.[Abstract/Free Full Text]

[2] Morillo CA, Klein GJ, Jones DL, Guiraudon CM. Chronic rapid atrial pacing: structural, functional and electrophysiological characteristics of a new model of sustained atrial fibrillation. Circulation (1995) 91:1588–95.[Abstract/Free Full Text]

[3] Daoud EG, Bogun F, Goyal R, Harvey M, Ching Man K, Adam Strickberger S, et al. Effects of atrial fibrillation on atrial refractoriness in humans. Circulation (1996) 94:1600–06.[Abstract/Free Full Text]

[4] Zhang S, Sawanobori T, Hirano Y, Hiraoka M. Multiple modulations of action potential duration by different calcium channel blocking agents in guinea pig ventricular myocytes. J Cardiovasc Pharmacol (1997) 30:489–96.[CrossRef][Web of Science][Medline]

[5] Michelucci A, Bagliani G, Colella A, Pieragnoli P, Porciani MC, Gensini G, et al. P wave assessment: state of the art update. Card Electrophysiol Rev (2002) 6:215–20.[CrossRef][Medline]

[6] Wang J, Liu L, Feng J, Nattel S. Regional and functional factors determining induction and maintenance of atrial fibrillation in dogs. Am J Physiol (1996) 271:H148–58.[Web of Science][Medline]

[7] Fareh S, Villemaire C, Nattel S. Importance of refractoriness heterogeneity in the enhanced vulnerability to atrial fibrillation induction caused by tachycardia-induced atrial electrical remodeling. Circulation (1998) 83:2202–9.

[8] Haissaguerre M, Jais P, Shah DC, Takahashi A, Hocini M, Quiniou G, et al. Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. N Engl J Med (1998) 339:659–66.[Abstract/Free Full Text]

[9] Ramanna H, Haner RN, Wittkampf FH, de Bakker JM, Wever EF, Elvan A, et al. Identification of the substrate of atrial vulnerability in patients with idiopathic atrial fibrillation. Circulation (2000) 101:995–1001.[Abstract/Free Full Text]

[10] Li D, Zhang L, Kneller J, Nattel S. Potential ionic mechanism for repolarization differences between canine right and left atrium. Circulation Res (2001) 88:1168–75.[Abstract/Free Full Text]

[11] Spach MS, Dolber PC, Heidlage JF. Interaction of inhomogeneities of repolarization with anisotropic propagation in dogs atria. A mechanism for both preventing and initiating reentry. Circ Res (1989) 65:1612–1631.[Abstract/Free Full Text]

[12] Spach MS, Dolber PC, Anderson PA. Multiple regional differences in cellular properties that regulate repolarization and contraction in the right atrium of adult and newborn dogs. Circ Res (1989) 65:1594–611.[Abstract]

[13] Garrey WE. The nature of fibrillary contraction of the heart-its relation to tissue mass and form. Am J Physiol (1914) 33:397–414.[Free Full Text]

[14] Chen SA, Hsich MH, Tai CT, Tsai CF, Prakash VS, Yu WC, et al. Initiation of atrial fibrillation by ectopic beats originating from the pulmonary veins: electrophysiological characteristics, pharmacological responses, and effects of radiofrequency ablation. Circulation (1999) 100:1879–86.[Abstract/Free Full Text]

[15] Lee SH, Lin FY, Yu WC, Cheng JJ, Kuan P, Hung CR, et al. Regional differences in the recovery course of tachycardia induced changes of atrial electrophysiological properties. Circulation (1999) 99:1255–64.[Abstract/Free Full Text]

[16] Oral H, Ozaydin M, Tada H, Chugh A, Scharf C, Hassan S, et al. Mechanistic significance of intermittent pulmonary vein tachycardia in patients with atrial fibrillation. J Cardiovasc Electrophysiol (2002) 13:645–50.[CrossRef][Web of Science][Medline]

[17] Kumagai K, Ogawa M, Noguchi H, Yasuda T, Nakashima H, Saku K, et al. Electrophysiological properties of pulmonary veins assessed using a multielectrode basket catheter. J Am Coll Cardiol (2004) 43:2281–9.[Abstract/Free Full Text]

[18] Chugh A, Ozaydin M, Scharf C, Lai Steve WK, Hall B, Cheung P, et al. Mechanism of immediate reccurences of atrial fibrillation after restoration of sinus rhythm. Pacing Clin Electrophysiol (2004) 27:77–82.[CrossRef][Medline]

[19] Gaspo R, Bosch RF, Talajic M, Nattel S. Functional mechanisms underlying tachycardia-induced sustained atrial fibrillation in a chronic dog model. Circulation (1997) 96:4027–35.[Abstract/Free Full Text]

[20] Elvan A, Wylie K, Zipes DP. Pacing-induced chronic atrial fibrillation impairs sinus node function in dogs. Electrophysiological remodeling. Circulation (1996) 94:2953–60.[Abstract/Free Full Text]

[21] Yue L, Feng J, Gaspo R, Li G-R, Wang Z, Nattel S, et al. Inonic remodeling underlying action potential changes in a canine model of atrial fibrillation. Circ Res (1997) 81:512–25.[Abstract/Free Full Text]


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