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(Circulation. 1999;100:876-883.)
© 1999 American Heart Association, Inc.
Basic Science Reports |
Relation Between Ligament of Marshall and Adrenergic Atrial Tachyarrhythmia
From the Division of Cardiology, Department of Medicine, Cedars-Sinai Medical Center, Los Angeles, Calif; the Department of Pathology (M.C.F.), UCLA School of Medicine, Los Angeles, Calif; and the Utah Valley Regional Medical Center (C.H.), Provo.
Correspondence to Peng-Sheng Chen, MD, Rm 5342, CSMC, 8700 Beverly Blvd, Los Angeles, CA 90048-1865. E-mail chenp{at}csmc.edu
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Abstract |
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Background—The mechanism of the adrenergic atrial tachyarrhythmia is unclear. We hypothesize that the ligament of Marshall (LOM) is sensitive to adrenergic stimulation and may serve as a source of the adrenergic atrial tachyarrhythmia.
Methods and Results—We performed computerized mapping studies in isolated-perfused canine left atrial tissues from normal dogs (n=9) and from dogs with chronic atrial fibrillation (AF) induced by 10 to 41 weeks of rapid pacing (n=3). Before isoproterenol, spontaneous activity occurred in only one normal tissue (cycle length, CL >1300 ms). During isoproterenol infusion, automatic rhythm was induced in both normal tissues (CL=578±172 ms) and AF tissues (CL=255±29 ms, P<0.05). The origin of spontaneous activity was mapped to the LOM. In the AF tissues, but not the normal tissues, we observed the transition from rapid automatic activity to multiple wavelet AF. Ablation of the LOM terminated the spontaneous activity and prevented AF. Immunocytochemical studies of the LOM revealed muscle tracts surrounded by tyrosine hydroxylase-positive (sympathetic) nerves.
Conclusions—We conclude that the LOM is richly innervated by sympathetic nerves and serves as a source of isoproterenol-sensitive focal automatic activity in normal canine atrium. The sensitivity to isoproterenol is upregulated after long-term rapid pacing and may contribute to the development of AF in this model.
Key Words: tachyarrhythmias • mapping • catecholamines • atrial fibrillation
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Introduction |
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The importance of catecholamines in the generation and maintenance of atrial fibrillation (AF) is recognized clinically; it is demonstrated by the relation of AF to states of increased adrenergic tone1 2 3 and by the use of ß-blockers in prophylaxis of AF after open-heart surgery.4 Coumel reported a clinical entity of adrenergic-mediated atrial tachyarrhythmia.5 In these patients, isoproterenol readily induces AF. The mechanism by which sympathetic stimulation facilitates the induction of atrial tachyarrhythmia and AF is unclear6 because sympathetic stimulation has no effect on atrial refractoriness.7 Although sympathetic stimulation may not shorten the refractory period, it is known that left cardiac sympathetic nerve stimulation can trigger an ectopic rhythm from the inferior left atrium.8 However, because only a few bipolar electrograms were registered in that study, the exact source of ectopic activity could not be determined. The purposes of this study were to use high-density computerized mapping techniques to determine the site of catecholamine-sensitive automatic foci in the left atrium of dogs and then study the activity of these automatic foci in a chronic canine AF model induced by rapid atrial pacing.9 10 The results were used to test the hypotheses that a specific atrial structure serves as the predominant origin of catecholamine-sensitive focal left atrial automaticity, and that in atria after long-term rapid pacing, this focal activity is upregulated and results in the induction of AF.
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Methods |
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The following research protocol was approved by the Institutional Animal Care and Use Committee and conforms to the American Heart Association guidelines.
Protocol 1: Studies of Normal Healthy Dogs In Vitro
Tissue Preparation
Nine mongrel dogs (18 to 25 kg) were placed under general
anesthesia with sodium pentobarbital (30 to 35 mg/kg IV),
intubated, and ventilated with room air by a respirator. The hearts
were rapidly excised. The left circumflex artery was selectively
cannulated and perfused with oxygenated Tyrode's solution
at 36.5°C. The Tyrode's solution has the following ionic
concentrations (in mmol/L): Dextrose 5.5, NaCl 125, KCl 4.5,
NaH2PO4 1.8,
CaCl2 2.7, MgCl2 0.5, and
NaHCO3 24.11 The posterior left
atrium along with a small portion of the basal left ventricle was
excised. The pulmonary veins were removed and were not included
in the preparation. The distal portion of the circumflex artery and all
large marginal arteries were ligated. The cut surface of
ventricular tissue was cauterized. The preparation was then
placed in the tissue bath and was perfused at 15 mL/min. The
endocardial surface was placed on a high-density mapping plaque with
509 bipolar recording channels built into the bottom of the
tissue chamber.11 12 A bipolar pacing electrode, a roving
bipolar recording electrode and a widely-spaced pair of bipolar
electrode (the pseudo ECG) were placed on the epicardial surface. In 3
of the dogs at the end of the study, a smaller high-density plaque was
placed on the epicardial surface over the area of earliest activation
to perform simultaneous epi- and endocardial mapping. The
small plaque contains 96 bipolar electrodes with 3.0 interelectrode
distance and covers an area measuring 2.1 cm by 2.1 cm. The tissue was
paced at a cycle length (CL) of 500 to 600 ms for 10 minutes before
data collection. In 2 of the dogs, the ligament of Marshall
(LOM)8 13 was excised at the end of study to determine
whether or not the induced rhythm would terminate and if other
subsidiary pacemakers were present.
Electrophysiological Study
The tissues were observed for spontaneous activity at baseline
for 5 minutes. If no spontaneous activity was seen, an attempt to
induce arrhythmia was made with programmed stimulation
including 8-beat baseline pacing train (S1) at
300 and 400 ms CL, followed by up to 3 premature stimuli or by burst
pacing at CL of 160 to 400 ms. Afterward, isoproterenol (4
µmol/L and 8 µmol/L) was added to the perfusate and
the above protocol was repeated. Sustained atrial arrhythmia
was defined by atrial activity of >30 beats in duration and a CL of
<3000 ms. Attempts were made to overdrive-suppress the rhythm with
rapid pacing.
Activation Mapping
The recording electrodes were connected to a
computerized mapping system (EMAP, Uniservices).12
Individual bipolar electrograms were analyzed12
and the patterns of activation were visualized either by isochronal
maps or by dynamic display.14 15 Continuous
recordings of epicardial bipolar electrograms and pseudo ECG
were acquired by the AXON TL-1 to 40 A/D system (Axon Instrument).
Protocol 2: Studies of Dogs With Pacing-Induced Chronic Atrial
Fibrillation
Three mongrel dogs of either sex (18 to 25 kg) were used. An
atrial pacing lead was inserted into the right atrial appendage and
connected to a Medtronic Itrel II 7424 neurostimulator implanted in a
subcutaneous pocket. After approximately 1 week, the pulse generator
was programmed to burst pace at a CL of 50 ms for 3 s with an
output of 3.0 volts, followed by a 5-s period without pacing. Digoxin
(0.25 mg/d) was given to control ventricular rate. The
animals were checked periodically for the presence of sustained AF
(>24 hours) off pacing. In these 3 dogs, sustained AF was documented
at 10, 41, and 11 weeks, respectively, after the first surgery. The
animals then underwent the same
electrophysiological studies as described
in Protocol 1. The third dog also underwent radiofrequency catheter
ablation of the left atrial epicardial surface at the LOM before
excising the heart. The radiofrequency energy was applied with a
standard 4-mm tip ablation catheter connected to a Radionic 3C
radiofrequency current generator. The power was set at 20 to 30 Watts,
and the duration of each application was 1 minute. Multiple
applications were performed along the LOM until the entire ligament was
ablated.
Histological Examination
The atrial tissues were fixed in 10% formalin, processed
routinely, and stained with trichrome and the antibodies to
neurofilament and tyrosine hydroxylase. The tissues were examined under
light microscopy for the presence of an insulated atrial tract and the
sympathetic nerves within the LOM.
Statistical Analyses
Student's t tests were used to compare the CL before
and during isoproterenol infusion. P
0.05 was considered
significant.
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Results |
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Figure 1
shows the epicardial
surface of the posterior left atrium in 2 dogs. The LOM is seen with
varying prominence, ranging from a whitish, fatty-fibrous streak (panel
1) to a readily apparent ligamentous structure (panel 2). The sutures
were used to tie off the marginal branches of the circumflex
coronary artery except on LOM where a suture was used to mark
the location of the earliest activation.
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Protocol 1
Spontaneous activity was not demonstrated in 7 of the 9 tissues
before infusion with isoproterenol. The first dog demonstrated a single
atrial depolarization over the 5-minute period. The fifth exhibited
spontaneous activity that was slow and irregular, with the shortest CL
of 1300 ms. After infusion of 4 µmol/L isoproterenol, all 9
tissues exhibited spontaneous activity. The first tissue revealed only
occasional atrial depolarizations, and only after burst pacing did it
demonstrate any sustained activity or tachycardia. The
sustained rhythm after burst pacing was regular with a CL of 800 ms.
The remaining 8 tissues demonstrated sustained atrial rhythms that were
either regular or irregular, with the CL between 400 and 2500 ms. Once
the rhythm stabilized, the CL varied between 400 and 800 ms
(mean±SD=580±183 ms). Increasing the concentration of isoproterenol
to 8 µmol/L did not significantly change the CL of the
spontaneous activity. None of the tissues demonstrated
spontaneous or pacing-induced fibrillation-like activity.
LOM Recording During Pacing and During Automatic
Rhythm
In 3 normal dogs we used 2 bipolar hook electrodes to record
from the upper and lower LOM. An additional hook electrode was used to
register the activation from the left ventricle.
Simultaneous computerized mapping studies were done from
the endocardium. Figure 2 shows bipolar
recordings from one tissue. Panel A shows a small second
potential (arrow) following a large local atrial electrogram. During
isoproterenol infusion (B), small sharp potentials (arrows) precede the
local atrial electrogram. The CL between these sharp potentials
(activation of the LOM) gradually lengthened (rate decreased) soon
after the discontinuation of isoproterenol. Also note that the
conduction time from the atrial tissue into the LOM is short (small
interval between 2 deflections) and reliable (always maintaining a 1:1
conduction) (A). However, the conduction in the reverse direction was
slow and unreliable, with long intervals and frequent conduction blocks
(B). Similar sharp potentials were also observed in human
patients.16 17 The bipolar atrial electrogram recorded
by the electrodes on the LOM was as early as any electrogram
recorded on the endocardium. In the other 2 tissues studied,
isoproterenol resulted in the reversal of the 2 potentials. However, a
prolonged pause between the 2 potentials was not observed.
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Figure 3 shows a typical example of the
atrial activity after the administration of isoproterenol. In the
beginning, the activity was both slow and irregular. It then became
more regular with significantly shorter CLs (approximately 500 ms). The
tachycardia would then persist for up to 5 minutes. The
spontaneous activity could be suppressed by overdrive pacing (Figure 4), which is compatible with
automaticity. The earliest site of activation corresponded to the
inferior portion of the LOM in all tissues studied. A
representative isochronal map and bipolar
electrograms for the spontaneous rhythm in dog 5 are shown in Figure 5.
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800 ms. There is no evidence of suppression after pacing at 400 and
300 ms CL. However, pacing at 250 and 200 ms results in a secondary
pause of 7.5 and 14 s, respectively. PCL indicates pacing cycle
length; A, atrial activity; and V, far-field ventricular
activity.
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In tissues 3 to 5, we performed simultaneous endocardial
and epicardial mapping. In all tissues, we documented that the earliest
activity at both endocardial and epicardial sites arose from the area
marked by LOM. Figure 6 shows an example.
In that figure, the upper edge of the epicardial electrode array was
placed at the LOM. The earliest epicardial and endocardial activation
occurred at the same site, then propagated to the remaining atrial
tissues centrifugally. There was no evidence of epicardial reentry
during the isoproterenol-induced spontaneous activity.
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Excision of LOM in 2 tissues terminated spontaneous activity. An
example is shown in Figure 7. The left
panel shows the tissue preparation. The numbers 1 to 5 indicate the
segments of the LOM excised. The top line of the right panel shows
tachycardia with a CL of 400 ms during isoproterenol
infusion. Excision of the LOM resulted in the termination of sustained
tachycardia.
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Protocol 2
No spontaneous activity was observed without pacing. Following
infusion with 4 µmol/L isoproterenol, tachycardia
occurred in the 2 tissues without ablation. The CL ranged from 220 ms
to 300 ms (mean 255±29 ms). This CL was significantly shorter than the
tachycardia in normal tissues during 4 µmol/L
isoproterenol infusion (P<0.05). As in normal dogs, the
tachycardia had their origin in the area marked by the LOM.
In the third dog, which underwent in vivo ablation of the LOM, no
spontaneous activity was seen with or without isoproterenol
infusion.
In the first tissue, short runs of non-sustained fibrillation-like activity was inducible by burst pacing. The duration of these runs increased from 12±9 s (range 3 to 26 s) at baseline to 69±81 s (range 18 to 229 s) during isoproterenol infusion. In the second dog, fibrillation could not be induced before isoproterenol but sustained runs of fibrillation could be induced during infusion. The duration was 77±44 s (range 18 to 126 s). In these 2 tissues, isoproterenol facilitated induction of fibrillation-like activity and increased the duration. In a third tissue that underwent ablation of the LOM, short runs of fibrillation could be induced before isoproterenol (mean 5±2 s, range 3 to 7 s) but not afterward. The ablation lesion was nontransmural.
In addition to induced fibrillation, we registered multiple episodes in
which automatic activity originated from the LOM area triggered AF.
Figure 8 shows an example. The panel on
the left shows consecutive snapshots of the dynamic activation display,
initially showing focal activity from the LOM (1460 to 1500 ms),
followed by multiple wavelet fibrillation. The right panel shows that
spontaneous activity originating from the LOM results in a
tachycardia (first 3 cycles) with CL alternans, followed by
fibrillatory activity. This episode implies that spontaneous rapid
activity originating from the LOM plays a role in the induction of in
vitro AF. This phenomenon was seen only in the first 2 tissues from the
chronic AF model and not in any other tissues from normal healthy dogs
or the chronic AF dog that underwent in vivo ablation of the LOM.
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Histological Examination
Histological studies showed that the LOM contains
muscle tracts and abundant nerve bundles that are well insulated by
fibrofatty tissues. The majority of the nerve bundles stained positive
for tyrosine hydroxylase. Figure 9 shows
typical examples of the histological staining.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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This study has 4 major findings: 1) In isolated-perfused normal canine left atrium, isoproterenol infusion can induce a focal source of automatic activity from the LOM. Ablation of the LOM results in abolition of the ectopic focus from that site. 2) This automatic activity is upregulated in the canine model of rapid-pacing induced chronic AF. 3) During isoproterenol infusion, the rapid automatic activity can trigger the onset of in vitro AF. This latter phenomenon occurs only in the left atrium harvested from dogs with long-term pacing-induced AF and is not seen in the normal atrium. 4) Abundant tyrosine hydroxylase-positive nerves are present in the LOM.
Ligament of Marshall and the Left Atrial Ectopic Rhythm
In 1850, Marshall13 described the presence of a
"vestigial fold of the pericardium" which had until then escaped
attention. This fold is a developmental vestige of the left primitive
veins. The location of the vestigial fold is in the back of the left
auricle, running from the coronary sinus upward to the region
of left superior pulmonary vein. Marshall reported that
"besides a duplicate of a serous layer of the pericardium, including
cellular and fatty tissue, the vestigial fold contains some fibrous
bands, small blood vessels and nervous filaments." He also observed
that this vestigial structure is connected to the small oblique
auricular vein that drains into the coronary sinus. Scherlag et
al8 performed a detailed study on the electrical activity
of the left atrial tract within the LOM in dogs. They found that the
bipolar electrogram near the LOM showed 2 deflections. During
sinus rhythm, the second of the 2 deflections originated from the
insulated tract. However, during left cardiac sympathetic nerve
stimulation, ectopic rhythm was induced and the activation sequence of
these 2 deflections was reversed. Because only a limited number of
recording channels were available, the exact location of the
ectopic focus was not determined.
In this study, we performed multichannel mapping of the isolated-perfused left atrium. The results showed that the automatic focus in the left atrium was dormant at baseline but became active during isoproterenol infusion. Furthermore, the ectopic rhythm always originated in the area near the LOM. These findings imply that the LOM may have significant clinical importance. Furthermore, because the LOM is an easily identifiable anatomical structure, it is an ideal target for ablative therapy.
Left Atrial Ectopic Rhythm and Paroxysmal Atrial
Fibrillation
Mirowski et al18 19 documented the presence of
automatic focus in the left atrium of both dogs and humans. These left
atrial automatic mechanisms may sometimes result in clinically
important arrhythmias.20 The exact location of the
automatic rhythm was not determined. However, one of the possible sites
was the sinocaval area in the left atrium where transmembrane potential
recordings consistently showed slight
diastolic depolarizations.21 The rabbit left
sinocaval area used in that study roughly corresponded to the
coronary sinus and may include its tributaries.
The development of radiofrequency catheter ablation provided new
insights into the mechanisms of atrial tachyarrhythmia.
Tracy et al22 and Kay et al23 performed
radiofrequency ablation in patients with ectopic atrial
tachycardia. They found that in a few patients, the sites
of origin of ectopic atrial tachycardia were in the left
atrium posterior wall, near the orifice of the pulmonary veins.
More recently, Haissaguerre et al17 reported that the
ectopic beats originating from the pulmonary veins may serve as
a source of ectopic activity that leads to spontaneous AF. Among the 4
pulmonary veins, the left superior pulmonary vein
(which is adjacent to the LOM) is by far the most common one that
generates ectopic atrial activity. The electrograms registered in our
study from the LOM (Figure 2
) are similar to that registered
from the left superior pulmonary vein by Haissaguerre et
al17 and by us.16 In the latter reports, 2
deflections similar to that shown in Figure 2 were found at the
orifice and inside the left superior pulmonary vein. During
atrial ectopic activity or at the onset of paroxysmal AF, the
morphology of the 2 deflections reversed. The sharp local activity was
followed after a long pause (>100 ms) by the local atrial activity,
with intermittent Wenckebach-type conduction blocks between the 2.
Although the similarity of the electrograms is not a definitive proof
of a causal relation, these findings suggest a possible role of LOM in
the generation and maintenance of paroxysmal AF in humans.
Adrenergic Atrial Tachyarrhythmia
A second clinical implication of our study is that the LOM may
serve as a structure that facilitates the induction of AF during
adrenergic (sympathetic) stimulation. Coumel et al5
reported a small group of patients in whom AF occurs predominantly in
the daytime, with evidence of adrenergic over-activity (such as
accelerated heart rate) before the onset of AF. In this latter group of
patients, isoproterenol infusion results in the induction of AF. In the
present study we demonstrated that the ectopic foci in the left
atrium is sensitive to sympathetic stimulation. This finding implies
that the LOM, with its rich sympathetic nerve distribution and the
proximity of these nerves to an isolated muscle bundle, may serve as a
source of adrenergic atrial tachyarrhythmias.
Other possible sources of adrenergic atrial tachyarrhythmias included structures in the right atrium, especially in the tissues near sinus node and the crista terminalis.24 Although crista terminalis is often the source of focal right atrial tachycardia,25 it rarely serves as the origin of focal AF.17
Implications on the Mechanisms of Chronic Atrial
Fibrillation
A third clinical implication of our study is that the LOM may play
a role in the induction of chronic AF. It was recently demonstrated
that intermittent or persistent rapid atrial pacing can result in
electrical remodeling of the atria and converting nonsustained AF into
sustained AF.9 10 Ectopic rhythm from the LOM could serve
as the source of the intermittent rapid atrial activity that results in
electrical remodeling of the remaining atria. This remodeling may
eventually lead to sufficient remodeling and chronic AF. Furthermore,
we have also observed that isoproterenol infusion in an atrium already
remodeled by rapid pacing can first trigger atrial
tachycardia from the LOM, followed by an abrupt transition
to AF. These findings imply that the LOM may serve as the source of
ectopic atrial tachycardia, which converts sinus rhythm to
AF after successful cardioversion.
Limitations
A limitation of this study is that the pulmonary veins
were not included in the preparation. It is unclear whether or not
pulmonary veins also contain pacemaker cells that are sensitive
to adrenergic stimulation.
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Acknowledgments |
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This study was undertaken during the tenure of a Fellowship Grant from the Department of Medicine, Korea University (to Y.-H.K.); a NIH CIDA (to J.J.C.O.) (HL-03611); a Cedars-Sinai ECHO Foundation Award (to H.S.K.); and a Pauline and Harold Price Endowment to (P.-S.C.); and was supported in part by NIH SCOR grant in Sudden Death (P50-HL52319), an AHA Greater Los Angeles Affiliate Grant-in-Aid (1114-G12), and the Ralph M. Parsons Foundation, Los Angeles, Calif. The authors thank Dr Rahul Mehra and Medtronic Inc for providing the pacemakers used in the study. We also thank Nina Wang, Dustan Morgan, Avile McCullen, Pei-Li Yan, and Meiling Yuan for their technical assistance and Elaine Lebowitz for her secretarial assistance.
Received December 22, 1998; revision received April 21, 1999; accepted April 22, 1999.
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M. Hirose and K. R. Laurita Calcium-mediated triggered activity is an underlying cellular mechanism of ectopy originating from the pulmonary vein in dogs Am J Physiol Heart Circ Physiol, April 1, 2007; 292(4): H1861 - H1867. [Abstract] [Full Text] [PDF]
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K. Nanthakumar, Y. R. Lau, V. J. Plumb, A. E. Epstein, and G. N. Kay Electrophysiological Findings in Adolescents With Atrial Fibrillation Who Have Structurally Normal Hearts Circulation, July 13, 2004; 110(2): 117 - 123. [Abstract] [Full Text] [PDF]
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A. M. Park, C.-C. Chou, P. C. Drury, Y. Okuyama, A. Peter, A. Hamabe, Y. Miyauchi, R. M. Kass, H. S. Karagueuzian, M. C. Fishbein, et al. Thoracic vein ablation terminates chronic atrial fibrillation in dogs Am J Physiol Heart Circ Physiol, June 1, 2004; 286(6): H2072 - H2077. [Abstract] [Full Text] [PDF]
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C.-C. Chou, S. Zhou, Y. Miyauchi, H.-N. Pak, Y. Okuyama, M. C. Fishbein, H. S. Karagueuzian, and P.-S. Chen Effects of procainamide on electrical activity in thoracic veins and atria in canine model of sustained atrial fibrillation Am J Physiol Heart Circ Physiol, May 1, 2004; 286(5): H1936 - H1945. [Abstract] [Full Text] [PDF]
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L.-F. Hsu, P. Jais, D. Keane, J. M. Wharton, I. Deisenhofer, M. Hocini, D. C. Shah, P. Sanders, C. Scavee, R. Weerasooriya, et al. Atrial Fibrillation Originating From Persistent Left Superior Vena Cava Circulation, February 24, 2004; 109(7): 828 - 832. [Abstract] [Full Text] [PDF]
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W.-S. Lin, C.-T. Tai, M.-H. Hsieh, C.-F. Tsai, Y.-K. Lin, H.-M. Tsao, J.-L. Huang, W.-C. Yu, S.-P. Yang, Y.-A. Ding, et al. Catheter Ablation of Paroxysmal Atrial Fibrillation Initiated by Non-Pulmonary Vein Ectopy Circulation, July 1, 2003; 107(25): 3176 - 3183. [Abstract] [Full Text] [PDF]
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L. Padeletti, N. Musilli, M. C. Porciani, A. Colella, L. Di Biase, G. Ricciardi, P. Pieragnoli, A. Michelucci, and G. Gensini Atrial fibrillation and cardiac resynchronization therapy: the MASCOT study Europace, January 1, 2003; 5(s1): S49 - S54. [Abstract] [Full Text] [PDF]
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A. Goette, U. Lendeckel, and H. U Klein Signal transduction systems and atrial fibrillation Cardiovasc Res, May 1, 2002; 54(2): 247 - 258. [Abstract] [Full Text] [PDF]
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J. M.T. de Bakker, S. Y. Ho, and M. Hocini Basic and clinical electrophysiology of pulmonary vein ectopy Cardiovasc Res, May 1, 2002; 54(2): 287 - 294. [Abstract] [Full Text] [PDF]
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P.-S. Chen, T.-J. Wu, C. Hwang, S. Zhou, Y. Okuyama, A. Hamabe, Y. Miyauchi, C.-M. Chang, L. S. Chen, M. C. Fishbein, et al. Thoracic veins and the mechanisms of non-paroxysmal atrial fibrillation Cardiovasc Res, May 1, 2002; 54(2): 295 - 301. [Abstract] [Full Text] [PDF]
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C. Pappone, G. Oreto, S. Rosanio, G. Vicedomini, M. Tocchi, F. Gugliotta, A. Salvati, C. Dicandia, M. P. Calabro, P. Mazzone, et al. Atrial Electroanatomic Remodeling After Circumferential Radiofrequency Pulmonary Vein Ablation: Efficacy of an Anatomic Approach in a Large Cohort of Patients With Atrial Fibrillation Circulation, November 20, 2001; 104(21): 2539 - 2544. [Abstract] [Full Text] [PDF]
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T.-J. Wu, J. J. C. Ong, C.-M. Chang, R. N. Doshi, M. Yashima, H.-L. A. Huang, M. C. Fishbein, C.-T. Ting, H. S. Karagueuzian, and P.-S. Chen Pulmonary Veins and Ligament of Marshall as Sources of Rapid Activations in a Canine Model of Sustained Atrial Fibrillation Circulation, February 27, 2001; 103(8): 1157 - 1163. [Abstract] [Full Text] [PDF]
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C.-M. Chang, T.-J. Wu, S. Zhou, R. N. Doshi, M.-H. Lee, T. Ohara, M. C. Fishbein, H. S. Karagueuzian, P.-S. Chen, and L. S. Chen Nerve Sprouting and Sympathetic Hyperinnervation in a Canine Model of Atrial Fibrillation Produced by Prolonged Right Atrial Pacing Circulation, January 2, 2001; 103(1): 22 - 25. [Abstract] [Full Text] [PDF]
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C. Pappone, S. Rosanio, G. Oreto, M. Tocchi, F. Gugliotta, G. Vicedomini, A. Salvati, C. Dicandia, P. Mazzone, V. Santinelli, et al. Circumferential Radiofrequency Ablation of Pulmonary Vein Ostia : A New Anatomic Approach for Curing Atrial Fibrillation Circulation, November 21, 2000; 102(21): 2619 - 2628. [Abstract] [Full Text] [PDF]
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Y.-J. Chen, S.-A. Chen, M.-S. Chang, and C.-I Lin Arrhythmogenic activity of cardiac muscle in pulmonary veins of the dog: implication for the genesis of atrial fibrillation Cardiovasc Res, November 1, 2000; 48(2): 265 - 273. [Abstract] [Full Text] [PDF]
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D. T. Kim, A. C. Lai, C. Hwang, L.-T. Fan, H. S. Karagueuzian, P.-S. Chen, and M. C. Fishbein The ligament of Marshall: a structural analysis in human hearts with implications for atrial arrhythmias J. Am. Coll. Cardiol., October 1, 2000; 36(4): 1324 - 1327. [Abstract] [Full Text] [PDF]
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C. Hwang, T.-J. Wu, R. N. Doshi, C. T. Peter, and P.-S. Chen Vein of Marshall Cannulation for the Analysis of Electrical Activity in Patients With Focal Atrial Fibrillation Circulation, April 4, 2000; 101(13): 1503 - 1505. [Abstract] [Full Text] [PDF]
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