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J Atr Fibrillation. 2010 Mar-May; 2(5): 231.
Published online 2010 Mar 1. doi: 10.4022/jafib.231
PMCID: PMC4956010
PMID: 28496651

Atrial Fibrillation in Athletes - The Story Behind The Running Hearts

Shaolong Li, MD,^1 Zhihui Zhang, MD,^2 Benjamin J Scherlag, PhD,^3
and Sunny S Po, MD, PhD^3

Shaolong Li

^1Department of Cardiology, Yun-Nan St.John Cardiology
Hospital,Yun-Nan, China(S.L.L)

Find articles by Shaolong Li

Zhihui Zhang

^2Department of Cardiology, The Third Xiangya Hospital of Central
South University, HuNan, China(Z.H.Z)

Find articles by Zhihui Zhang

Benjamin J Scherlag

^3Heart Rhythm Research Institute and Department of Medicine, the
University of Oklahoma Health Sciences Center, Oklahoma City (B.J.S.,
S.S.P.)

Find articles by Benjamin J Scherlag

Sunny S Po

^3Heart Rhythm Research Institute and Department of Medicine, the
University of Oklahoma Health Sciences Center, Oklahoma City (B.J.S.,
S.S.P.)

Find articles by Sunny S Po
Author information Article notes Copyright and License information
Disclaimer
^1Department of Cardiology, Yun-Nan St.John Cardiology
Hospital,Yun-Nan, China(S.L.L)
^2Department of Cardiology, The Third Xiangya Hospital of Central
South University, HuNan, China(Z.H.Z)
^3Heart Rhythm Research Institute and Department of Medicine, the
University of Oklahoma Health Sciences Center, Oklahoma City (B.J.S.,
S.S.P.)
Correspondence to: Sunny S. Po, M.D., Ph.D, Heart Rhythm Institute,
University of Oklahoma Health Sciences Center. 1200 Everett Drive,
Room ET6E103, Oklahoma City, OK 73104, US.
Received 2009 Nov 12; Revised 2010 Feb 18; Accepted 2010 Feb 24.
Copyright notice
This article has been cited by other articles in PMC.

Introduction

Atrial fibrillation (AF) is the most commonly encountered arrhythmia
in clinical practice but the mechanisms underlying the initiation and
maintenance of AF are yet to be clarified. It is wellknown that
regular exercise is beneficial to health and reduces the risks of
cardiovascular diseases. However, recent studies suggest that
long-term endurance exercise, including running, swimming, rowing and
cycling, or vigorous competitive sports may increase the incidence of
AF in these athletes.[1-3] Since different studies used different
criteria to define the intensity of exercise, the association between
exercise and AF in people who exercise simply for fitness is not well
established. For instance, in the Cardiovascular Health Study, the
incidence of AF in older adults (>65 years old) was lower with
moderate-intensity but not high-intensity exercise.[4] In the
Physician Health Study, vigorous exercise, defined as any exercise
strenuous enough to break sweat, was associated with an increase in
the incidence of AF only in joggers younger than 55 years old.[5]
However, how much exercise is too much remains debatable. This review
article is intended to provide a summary of the possible links
between vigorous exercise and AF that occurs in endurance or
competitive athletes.

Exercise and AF

It is widely accepted that regular aerobic exercise reduces
cardiovascular risks.[4-9] For instance, moderate physical activities
can reduce the incidence of AF in elderly people.[4] However, people
who practice competitive sports or endurance sports have a higher
incidence of developing AF in the absence of structural heart
diseases (lone AF). Elosua et aL.[9] discovered that if the
cumulative hours of life-time sports activities are longer than 1500
hours, there is an increased incidence of lone AF in these subjects.
Another study by Mont et al.[2] showed an increase in AF incidence if
the subjects practiced more than 3 hours of endurance sports weekly
for more than two years. A study[1] on the incidence of lone AF in
marathon runners, in comparison to sedentary men, demonstrated a
higher incidence of AF in runners (annual incidence: 0.43/100 for
runners, 0.11/100 for sedentary men). Karjalainen et al.[10] followed
a group of elite male orienteers (N=300, 35-59 of age) and 495 age
and gender matched control for 10 years. They found that although the
mortality of the orienteers was much lower than controls (1.7% vs.
8.5%), the incidence of AF was much higher (5.3% vs. 0.9%). All these
aforementioned studies suggest that the incidence of AF in male
athletes is 1.8-8.8 folds higher than sedentary men.[1,2,9,10,11]

Characteristics of AF in Athletes

AF in endurance athletes appears to have the following
characteristics.[14-16] First, they are typically young or
middle-aged adults and have practiced endurance sports for several
years. Several studies[9-13] indicate that young or middle-aged
athletes who had undergone longterm high intensity training have the
highest incidence of AF. Second, it is more prevalent in male than
female athletes. Furlanello et al.[12] followed 146 young elite
athletes who had arrhythmia problems (male: 122, female: 24) for a
mean of 62 months. In the 13 athletes who developed AF, all of them
were male. Third, AF often occurs at night or after meal and less
frequently during exercise, which implies that AF in endurance
athletes may be related to increased vagal tone.[14] However, AF does
occur in endurance athletes during exercise, suggesting that the role
of the sympathetic tone cannot be ignored. Fourth, lone, paroxysmal
AF in endurance athletes can progress to persistent AF, in contrast
to what was originally described.[14] Hoogasteen et al.[13] found
that 17% exercise-related paroxysmal AF progressed to persistent AF.
This finding was later verified by the GIRAFA study[15] showing that
43% patients with exercise-related AF were in persistent AF.

The Mechanisms Underlying Exerciserelated AF

Exercise and The Autonomic Nervous System

Although high vagal tone manifesting as sinus bradycardia and
asymptomatic AV conduction delay in well-trained athletes has been
known for decades, clues suggesting the relationship between the
autonomic nervous system (ANS) and AF in athletes originally came
from the striking resemblance of the typical symptoms of this type of
AF and the "vagal AF" originally described by Coumel.[14] The
classical symptoms of "vagal AF" described by Coumel include: (1)
predominantly male between 30 and 50 of age, (2) usually occurs at
night and rarely occurs between breakfast and lunch when the
sympathetic tone is high, (3) rarely occurs during exercise or
emotional stress, (4) relaxation following stress frequently triggers
AF and (5) AF is often preceded by bradycardia lasting from seconds
to hours. Since vagal stimulation had been used to induce AF for
nearly a century, a logic explanation for AF in athletes is that
chronic exercise "tunes" the ANS to be vagally predominant, which in
turn triggers paroxysmal AF. However, this hypothesis has not been
proven and "vagal AF" continues to be viewed as a rare form of AF
that only occurs in a very small population of AF patients, such as
endurance athletes.

The heart is richly innervated by the autonomic nervous system (ANS).
The cardiac ANS can be divided into the extrinsic and intrinsic
components. The former consists of the soma in brain nuclei and
chains of ganglia along the spinal cord and the axons that course en
route to the heart. The latter is composed of a neural network formed
by axons and autonomic ganglia concentrated at the ganglionated plexi
(GP) embedded within epicardial fat pads on the heart itself. The
intrinsic cardiac ANS functions as the "little brain" on the heart as
proposed by Armour et al.[17]

In the past decade, the role of the cardiac ANS in the initiation and
maintenance of AF has been actively investigated. Several basic and
clinical studies have indicated that the initiation of paroxysmal AF
requires the activation of both the sympathetic and parasympathetic
components of the cardiac ANS,[18-21] indicating that perhaps some
degree of sympathetic influence may play a cooperative role in the
initiation of "vagal AF." Autonomic denervation has been shown in
multiple clinical and experimental studies to suppress AF.[22-24]
Unfortunately, there is no animal model that reproduces the type of
cardiac remodeling that is present in endurance athletes. Whether AF
in endurance athletes is associated with a hyperactive autonomic
state will require further basic and clinical studies.

Exercise and Atrial Enlargement (LAE)

Exercise increases the level of circulating catecholamine and leads
to a hyperdynamic state of the circulation. In athletes undergoing
long-term training, their hearts often develop adaptive changes such
as LAE, left ventricular hypertrophy and enlargement.[25] Increased
left atrial pressure leads to stretch of the left atrial wall,
resulting in shortening of the effective refractory period (ERP) and
increasing ERP dispersion, which in turn facilitates the initiation
and maintenance of AF. Using echocardiography, Pelliccia et al[26]
studied 1777 athletes with structurally normal hearts who
participated in 38 types of sport activities. The left atrial
dimension was larger than 40 mm in 347 subjects (20%) and larger than
45 mm in 38 subjects (2%). None of the athletes had LV wall motion
abnormality or reduced LV ejection fraction. Among the 38 sports, the
incidence of LAE was significantly increased in 28 sports,
particularly rowing (18%), cycling (10%), ice hockey (10%), rugby
(7%) and soccer (7%). Interestingly, athletes with LAE are more
likely to win an international competition (40%) than those without
LAE (20%). In athletes with LAE, 86% of them had an increased LV end
diastolic diameter (>55 mm), in contrast to 34% in athletes without
LAE. Although the incidence of AF in athletes was not different from
non-athletes, the authors concluded that LAE might be a physiological
adaptation to exercise. In contrast, another study by Mont et al[2]
found the LA dimension in former athletes, several years off vigorous
training, remained larger than control subjects (38.4+-6 mm vs. 34.5+-3
mm). Even years after vigorous training had been discontinued, the
incidence of AF in these former athletes remained higher than control
subjects. Whether LAE is an epiphenomenon of vigorous exercise or is
truly a risk factor for AF remains to be investigated.

Exercise and Inflammation

Studies have shown that excessive exercise induced inflammatory
responses in the body. For instance, excessive training may lead to
tissue injury and subsequently activates circulating monocytes, which
in turn produces large quantities of IL-1b, and/or IL-6, and/or TNF-a
and systemic inflammation.[27] In patients with lone AF, histological
examination of the atrium revealed inflammatory responses compatible
with the diagnosis of myocarditis in 66% of the patients.[28] Chung
et al[29] discovered that patients with AF <=24 hours had higher
C-reactive protein (CRP) levels than those in sinus rhythm.
Persistent AF patients had a higher CRP level than paroxysmal AF
patients and both groups had higher CRP levels than controls. That
study is the first to document elevated CRP in non-postoperative
arrhythmia patients. These findings were reinforced by a stepwise CRP
elevation with higher AF burden. Despite the correlation between
inflammation and AF, it remains unclear if inflammation helps
initiate or maintain AF or is only a by-product of AF. Moreover, the
relationship between exercise, inflammation and AF are yet to be
better understood.

The Relationship between the Cardiac ANS and AF in Athletes

The heart is richly innervated by the autonomic nervous system (ANS).
The cardiac ANS can be divided into the extrinsic and intrinsic
components. The former consists of the soma in brain nuclei and
chains of ganglia along the spinal cord and the axons that course en
route to the heart. The latter is composed of a neural network formed
by axons and autonomic ganglia concentrated at the ganglionated plexi
(GP) embedded within epicardial fat pads on the heart itself. The
intrinsic cardiac ANS functions as the "little brain" on the heart as
proposed by Armour et al.[29] As discussed before, endurance athletes
have the propensity for an elevated vagal tone, a higher level of
biomarkers for inflammation and dilated atria. The one-million dollar
question is: "What is the common trigger and substrate which help
initiate and maintain AF in endurance athletes?" Atrial stretch in a
dilated atrium is capable of abbreviating the atrial action potential
and effective refractory period (ERP) as well as an increasing the
ERP dispersion, providing an ideal reentry substrate for AF. However,
a timely spontaneous premature beat (trigger) from the PV or non-PV
site is still required to initiate AF in atria that have been
preconditioned as a reentry substrate. An attractive candidate that
provides both the trigger and substrate is a hyperactive state of the
cardiac autonomic nervous system.[21] Activation of the
parasympathetic elements shortens the action potential and effective
refractory period of the atrium and PV whereas activation of the
sympathetic elements provides a larger Ca++ transient.[20] A
synergistic action of the sympathetic and parasympathetic elements
can lead to early after depolarizations and subsequently spontaneous
premature depolarizations (triggers). Meanwhile, a hyperactive state
of the cardiac ANS may have already prepared a substrate for reentry
which is caused by an increased dispersion of the refractoriness as a
result of the heterogeneous innervation of the heart by the cardiac
ANS.[20-22] Moreover, cardiac ANS also activates bradykinins and
interleukins that can lead to inflammation.[30] In other word, the
cardiac ANS may serve as the common facilitator for the dynamics of
AF initiation and maintenance in athletes. Future studies will be
needed to examine the role of the cardiac ANS in AF among athletes to
develop a selective therapy to treat them.

Treatment for AF in Athlete

The first step to treat AF in athletes is to exclude other medical
conditions that may predispose endurance athletes to AF, such as
hyperthyroidism and pericarditis.[31-34] Substances such as cocaine,
caffeine, anabolic steroids and sympathomimetics in cold medicines
should be discontinued.[32,33] In addition, structural heart diseases
or other cardiac arrhythmic (e.g. Wolff-Parkinson-White syndrome,
hypertrophic cardiomyopathy, long QT syndrome) should be excluded.[33
,34] As the mechanisms underlying AF in endurance athletes are not
well understood, management of this type of AF is mainly based on
limited evidence-based studies and therefore remains controversial.
The following recommendations are proposed by the Study Group on
Sports Cardiology of the European Association for Cardiovascular
Prevention and Rehabilitation.[33]

After all the contributing factors have been eliminated, it is
recommended that[33] athletes in early stage of paroxysmal AF
temporarily discontinue training for two months to stabilize sinus
rhythm. The degree of improvement during this resting period
determines if athletes can resume their training. In athletes without
other cardiac disorders, the recommendation for sports participation
also largely depends on the ventricular rate during AF. If history
reveals a high ventricular rate or hemodynamic instability during AF,
the athletes should be instructed to stop exercising on the emergence
of palpitation or related symptoms.[33] Such patients may need
medications that slow the ventricular rate, ideally at doses that do
not cause sinus bradycardia at rest or chronotropic incompetence
during exercise.

Of note, the Task Force 7 of the 36th Bethesda Conference recommended
that athletes with asymptomatic AF in the absence of structural heart
disease who maintain a ventricular rate that increases and slows
appropriately and is comparable to that of a normal sinus response in
relation to the level of activity, while receiving no therapy or
therapy with AV nodal-blocking drugs, can participate in all
competitive sports.[34] It remains to be determined if athletes with
symptomatic AF should discontinue training for two months to
stabilize sinus rhythm as recommended by the European task force.[33]

There is a theoretical risk of using b-block to treat this type of AF
as it may further slow the sinus rate and produces an unopposed
hyper-cholinergic state, which may indeed facilitate the formation of
AF. The use of class Ia or Ic agents to treat AF in athletes remains
to be clarified. Of note, AV nodal conduction can be enhanced during
atrial tachyarrhythmia. Using class Ia or Ic agents may convert AF to
atrial flutter, resulting in 1;1 conduction to the ventricle.
Therefore, AV nodal blocking agents such as a b-blocker or Ca++
channel blocker should always be used in conjunction with class Ia or
Ic agents.

Since the landmark report by Haissaguerre et al[35] indicating that
focal AF is often induced by rapid focal discharges originating from
the pulmonary veins and/or adjacent atrial tissue, catheter ablation
for AF has evolved to be the treatment of choice for drug-refractory
AF, particularly for paroxysmal AF. Furlanello et al36 performed
catheter ablation (PV isolation +- atrial flutter ablation) on 20 male
competitive athletes who had very symptomatic lone AF. Except for one
patient whose right inferior pulmonary vein could not be isolated,
all other patients had successful PV isolation in the first ablation
procedure. Interestingly, when all the patients were restudied, 62
(81%) of the previously isolated PVs have resumed conduction. Most
importantly, the incidence of conduction recurrence did not
correlated with the recurrence of AF, suggesting that the triggers
and/or substrate for AF in these patients are not limited to PVs and
adjacent atrial tissue. After 2.3 +- 0.4 ablation procedures, only two
athletes continued to have short episodes of AF during 36.1 +- 12.7
months of follow-up. The maximal exercise capacity also significantly
improved after ablation. Whether AF in endurance athletes responds
differently to ablation than non-athletes remains to be clarified. In
addition, AF in athletes may be related to a hyperactive state of the
ANS. Ablation targeting the ganglionated plexi along with PV
isolation theoretically may yield better results but it remains to be
proven.

Conclusions

The association between moderate-intensity exercise and AF remains
controversial. But in athletes undergoing high-intensity and
long-term exercise, this association appears to be much stronger. A
hyperactive state of the cardiac autonomic nervous system may play an
important role in the initiation and maintenance of AF in endurance
athletes.

Disclosures

None.

References

1. Molina Lluis, Mont Lluis, Marrugat Jaume, Berruezo Antonio,
Brugada Josep, Bruguera Jordi, Rebato Carolina, Elosua Roberto.
Long-term endurance sport practice increases the incidence of lone
atrial fibrillation in men: a follow-up study. Europace. 2008 May;10
(5):618-23. [PubMed] [Google Scholar]
2. Mont L, Sambola A, Brugada J, Vacca M, Marrugat J, Elosua R, Pare
C, Azqueta M, Sanz G. Long-lasting sport practice and lone atrial
fibrillation. Eur. Heart J. 2002 Mar;23 (6):477-82. [PubMed] [Google
Scholar]
3. Baldesberger Sylvette, Bauersfeld Urs, Candinas Reto, Seifert
Burkhardt, Zuber Michel, Ritter Manfred, Jenni Rolf, Oechslin Erwin,
Luthi Pia, Scharf Christop, Marti Bernhard, Attenhofer Jost Christine
H. Sinus node disease and arrhythmias in the long-term follow-up of
former professional cyclists. Eur. Heart J. 2008 Jan;29 (1):71-8. [
PubMed] [Google Scholar]
4. Mozaffarian Dariush, Furberg Curt D, Psaty Bruce M, Siscovick
David. Physical activity and incidence of atrial fibrillation in
older adults: the cardiovascular health study. Circulation. 2008 Aug
19;118 (8):800-7. [PMC free article] [PubMed] [Google Scholar]
5. Aizer Anthony, Gaziano J Michael, Cook Nancy R, Manson Joann E,
Buring Julie E, Albert Christine M. Relation of vigorous exercise to
risk of atrial fibrillation. Am. J. Cardiol. 2009 Jun 01;103 (11)
:1572-7. [PMC free article] [PubMed] [Google Scholar]
6. Morris J N, Everitt M G, Pollard R, Chave S P, Semmence A M.
Vigorous exercise in leisure-time: protection against coronary heart
disease. Lancet. 1980 Dec 06;2 (8206):1207-10. [PubMed] [Google
Scholar]
7. Blair S N, Kampert J B, Kohl H W, Barlow C E, Macera C A,
Paffenbarger R S, Gibbons L W. Influences of cardiorespiratory
fitness and other precursors on cardiovascular disease and all-cause
mortality in men and women. JAMA. 1996 Jul 17;276 (3):205-10. [PubMed
] [Google Scholar]
8. Thompson Paul D, Buchner David, Pina Ileana L, Balady Gary J,
Williams Mark A, Marcus Bess H, Berra Kathy, Blair Steven N, Costa
Fernando, Franklin Barry, Fletcher Gerald F, Gordon Neil F, Pate
Russell R, Rodriguez Beatriz L, Yancey Antronette K, Wenger Nanette
K. Exercise and physical activity in the prevention and treatment of
atherosclerotic cardiovascular disease: a statement from the Council
on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and
Prevention) and the Council on Nutrition, Physical Activity, and
Metabolism (Subcommittee on Physical Activity). Circulation. 2003 Jun
24;107 (24):3109-16. [PubMed] [Google Scholar]
9. Elosua Roberto, Arquer Andreu, Mont Lluis, Sambola Antonia, Molina
Lluis, Garcia-Moran Emilio, Brugada Josep, Marrugat Jaume. Sport
practice and the risk of lone atrial fibrillation: a case-control
study. Int. J. Cardiol. 2006 Apr 14;108 (3):332-7. [PubMed] [Google
Scholar]
10. Karjalainen J, Kujala U M, Kaprio J, Sarna S, Viitasalo M. Lone
atrial fibrillation in vigorously exercising middle aged men:
case-control study. BMJ. 1998 Jun 13;316 (7147):1784-5. [PMC free
article] [PubMed] [Google Scholar]
11. Heidbuchel Hein, Anne Wim, Willems Rik, Adriaenssens Bert, Van de
Werf Frans, Ector Hugo. Endurance sports is a risk factor for atrial
fibrillation after ablation for atrial flutter. Int. J. Cardiol. 2006
Feb 08;107 (1):67-72. [PubMed] [Google Scholar]
12. Furlanello F, Bertoldi A, Dallago M, Galassi A, Fernando F, Biffi
A, Mazzone P, Pappone C, Chierchia S. Atrial fibrillation in elite
athletes. J. Cardiovasc. Electrophysiol. 1998 Aug;9 (8 Suppl):S63-8.
[PubMed] [Google Scholar]
13. Hoogsteen Jan, Schep Goof, Van Hemel Norbert M, Van Der Wall
Ernst E. Paroxysmal atrial fibrillation in male endurance athletes. A
9-year follow up. Europace. 2004 May;6 (3):222-8. [PubMed] [Google
Scholar]
14. Coumel P. Paroxysmal atrial fibrillation: a disorder of autonomic
tone? Eur. Heart J. 1994 Apr;15 Suppl A ():9-16. [PubMed] [Google
Scholar]
15. Mont Lluis, Tamborero David, Elosua Roberto, Molina Irma,
Coll-Vinent Blanca, Sitges Marta, Vidal Barbara, Scalise Andrea,
Tejeira Alejandro, Berruezo Antonio, Brugada Josep. Physical
activity, height, and left atrial size are independent risk factors
for lone atrial fibrillation in middle-aged healthy individuals. 
Europace. 2008 Jan;10 (1):15-20. [PubMed] [Google Scholar]
16. Levy S, Maarek M, Coumel P, Guize L, Lekieffre J, Medvedowsky J
L, Sebaoun A. Characterization of different subsets of atrial
fibrillation in general practice in France: the ALFA study. The
College of French Cardiologists. Circulation. 1999 Jun 15;99 (23)
:3028-35. [PubMed] [Google Scholar]
17. Armour J A, Murphy D A, Yuan B X, Macdonald S, Hopkins D A. Gross
and microscopic anatomy of the human intrinsic cardiac nervous
system. Anat. Rec. 1997 Feb;247 (2):289-98. [PubMed] [Google Scholar]
18. Bettoni Marco, Zimmermann Marc. Autonomic tone variations before
the onset of paroxysmal atrial fibrillation. Circulation. 2002 Jun
11;105 (23):2753-9. [PubMed] [Google Scholar]
19. Amar David, Zhang Hao, Miodownik Saul, Kadish Alan H. Competing
autonomic mechanisms precede the onset of postoperative atrial
fibrillation. J. Am. Coll. Cardiol. 2003 Oct 01;42 (7):1262-8. [
PubMed] [Google Scholar]
20. Ogawa Masahiro, Zhou Shengmei, Tan Alex Y, Song Juan, Gholmieh
Ghassan, Fishbein Michael C, Luo Huai, Siegel Robert J, Karagueuzian
Hrayr S, Chen Lan S, Lin Shien-Fong, Chen Peng-Sheng. Left stellate
ganglion and vagal nerve activity and cardiac arrhythmias in
ambulatory dogs with pacing-induced congestive heart failure. J. Am.
Coll. Cardiol. 2007 Jul 24;50 (4):335-43. [PubMed] [Google Scholar]
21. Nattel Stanley. Combined parasympathetic-sympathetic nerve
discharge and pulmonary vein afterdepolarizations: a new unifying
concept with basic and clinical relevance. Heart Rhythm. 2005 Jun;2
(6):632-3. [PubMed] [Google Scholar]
22. Tan Alex Y, Zhou Shengmei, Ogawa Masahiro, Song Juan, Chu
Matthew, Li Hongmei, Fishbein Michael C, Lin Shien-Fong, Chen Lan S,
Chen Peng-Sheng. Neural mechanisms of paroxysmal atrial fibrillation
and paroxysmal atrial tachycardia in ambulatory canines. Circulation.
2008 Aug 26;118 (9):916-25. [PMC free article] [PubMed] [Google
Scholar]
23. Jayachandran J V, Sih H J, Winkle W, Zipes D P, Hutchins G D,
Olgin J E. Atrial fibrillation produced by prolonged rapid atrial
pacing is associated with heterogeneous changes in atrial sympathetic
innervation. Circulation. 2000 Mar 14;101 (10):1185-91. [PubMed] [
Google Scholar]
24. Pokushalov Evgeny, Romanov Alex, Shugayev Pavel, Artyomenko
Sergey, Shirokova Natalya, Turov Alex, Katritsis Demosthenes G.
Selective ganglionated plexi ablation for paroxysmal atrial
fibrillation. Heart Rhythm. 2009 Sep;6 (9):1257-64. [PubMed] [Google
Scholar]
25. Neilan Tomas G, Yoerger Danita M, Douglas Pamela S, Marshall Jane
E, Halpern Elkan F, Lawlor David, Picard Michael H, Wood Malissa J.
Persistent and reversible cardiac dysfunction among amateur marathon
runners. Eur. Heart J. 2006 May;27 (9):1079-84. [PubMed] [Google
Scholar]
26. Pelliccia Antonio, Maron Barry J, Di Paolo Fernando M, Biffi
Alessandro, Quattrini Filippo M, Pisicchio Cataldo, Roselli
Alessandra, Caselli Stefano, Culasso Franco. Prevalence and clinical
significance of left atrial remodeling in competitive athletes. J.
Am. Coll. Cardiol. 2005 Aug 16;46 (4):690-6. [PubMed] [Google Scholar
]
27. Smith L L. Cytokine hypothesis of overtraining: a physiological
adaptation to excessive stress? Med Sci Sports Exerc. 2000 Feb;32 (2)
:317-31. [PubMed] [Google Scholar]
28. Frustaci A, Chimenti C, Bellocci F, Morgante E, Russo M A, Maseri
A. Histological substrate of atrial biopsies in patients with lone
atrial fibrillation. Circulation. 1997 Aug 19;96 (4):1180-4. [PubMed]
[Google Scholar]
29. Chung M K, Martin D O, Sprecher D, Wazni O, Kanderian A, Carnes C
A, Bauer J A, Tchou P J, Niebauer M J, Natale A, Van Wagoner D R.
C-reactive protein elevation in patients with atrial arrhythmias:
inflammatory mechanisms and persistence of atrial fibrillation. 
Circulation. 2001 Dec 11;104 (24):2886-91. [PubMed] [Google Scholar]
30. Borovikova L V, Ivanova S, Zhang M, Yang H, Botchkina G I,
Watkins L R, Wang H, Abumrad N, Eaton J W, Tracey K J. Vagus nerve
stimulation attenuates the systemic inflammatory response to
endotoxin. Nature. 2000 May 25;405 (6785):458-62. [PubMed] [Google
Scholar]
31. Vergara Pasquale, Picardi Giuseppe, Nigro Gerardo, Scafuro
Francesco, de Chiara Annabella, Calabro Raffaele, Vergara Giuseppe.
Evaluation of thyroid dysfunction in patients with paroxysmal atrial
fibrillation. Anadolu Kardiyol Derg. 2007 Jul;7 Suppl 1 ():104-6. [
PubMed] [Google Scholar]
32. Sullivan M L, Martinez C M, Gallagher E J. Atrial fibrillation
and anabolic steroids. J Emerg Med. 1999 Sep 28;17 (5):851-7. [PubMed
] [Google Scholar]
33. Heidbuchel Hein, Panhuyzen-Goedkoop Nicole, Corrado Domenico,
Hoffmann Ellen, Biffi Allessandro, Delise Pietro, Blomstrom-Lundqvist
Carina, Vanhees Luc, Ivarhoff Per, Dorwarth Uwe, Pelliccia Antonio.
Recommendations for participation in leisure-time physical activity
and competitive sports in patients with arrhythmias and potentially
arrhythmogenic conditions Part I: Supraventricular arrhythmias and
pacemakers. Eur J Cardiovasc Prev Rehabil. 2006 Aug;13 (4):475-84. [
PubMed] [Google Scholar]
34. Zipes Douglas P, Ackerman Michael J, Estes N A Mark, Grant
Augustus O, Myerburg Robert J, Van Hare George. Task Force 7:
arrhythmias. J. Am. Coll. Cardiol. 2005 Apr 19;45 (8):1354-63. [
PubMed] [Google Scholar]
35. Haissaguerre M, Jais P, Shah D C, Takahashi A, Hocini M, Quiniou
G, Garrigue S, Le Mouroux A, Le Metayer P, Clementy J. Spontaneous
initiation of atrial fibrillation by ectopic beats originating in the
pulmonary veins. N. Engl. J. Med. 1998 Sep 03;339 (10):659-66. [
PubMed] [Google Scholar]
36. Furlanello Francesco, Lupo Pierpaolo, Pittalis Mario, Foresti
Sara, Vitali-Serdoz Laura, Francia Pietro, De Ambroggi Guido, Ferrero
Paolo, Nardi Stefano, Inama Giuseppe, De Ambroggi Luigi, Cappato
Riccardo. Radiofrequency catheter ablation of atrial fibrillation in
athletes referred for disabling symptoms preventing usual training
schedule and sport competition. J. Cardiovasc. Electrophysiol. 2008
May;19 (5):457-62. [PubMed] [Google Scholar]
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