Current updates

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Atrial fibrillation and atrial flutter in athletes
Naiara Calvo,1 Josep Brugada,2 Marta Sitges,2 Lluís Mont2
OPEN ACCESS
1
Arrhythmia Unit, Department ABSTRACT associated with AF in healthy middle-aged men.
of Cardiology and Atrial fibrillation (AF) is the most common arrhythmia in They evaluated AF prevalence in veteran male
Cardiovascular Surgery,
University of Navarra, Navarra,
clinical practice, with an estimated prevalence of 0.4% to orienteers and in a matched control group. LAF
Pamplona, Spain 1% in the general population, increasing with age to 8% was diagnosed in 12 of 228 (5.3%) orienteers and
2
Thorax Institute, Hospital in those above 80 years. The recognised risk factors for in 2 of 212 (0.9%) controls (who also engaged in
Clínic, University of Barcelona, developing AF include age, structural heart disease, vigorous exercise) ( p=0.012), the relative risk
Institut d’Investigació Biomèdica hypertension, diabetes mellitus or hyperthyroidism. being 5.5 (95% CI 1.3 to 24.4) in orienteers. Our
August Pi i Sunyer (IDIBAPS),
Barcelona, Catalonia, Spain However, the mechanisms underlying the initiation of AF group analysed 1160 consecutive patients seen at
in patients below 60 years of age, in whom no the Outpatient Arrhythmia Clinic between
Correspondence to cardiovascular disease or any other known causal factor October 1997 and March 1999. The proportion of
Dr Lluís Mont, Thorax Institute is present, remain to be clarified. This condition, termed sport activity among patients with LAF was sig-
(ICT)—Cardiology Department,
Hospital Clinic, University of
as lone AF, may be responsible for as many as 30% of nificantly higher than among men from the
Barcelona, Villarroel 170, patients with paroxysmal AF seeking medical attention. general population in Catalonia (62.7% vs
Barcelona 08036, Catalonia, Recent studies suggest that long-term endurance 15.4%).10 Regular sport activity was defined as
Spain; exercise may increase the incidence of AF and atrial high-intensity practice for at least 3 h a week for
[email protected] flutter (AFl) in this population. This review article is 2 years. An age-matched study including the same
Accepted 30 May 2012 intended to analyse the prevalence of AF and AFl, the population of athletic men with LAF and age-
pathophysiological mechanisms responsible for the matched controls selected from the general popula-
association between endurance sport practice and AF or tion of Girona, using data from the REGICOR
AFl and the recommended therapeutic options in (Registre Gironí del Cor) Study, confirmed that
endurance athletes. current and prolonged sport practice, defined as
more than 1500 lifetime hours of intense endur-
ance practice, was associated with a three times
INTRODUCTION higher prevalence of LAF, and with five times
Atrial fibrillation (AF) is the most common clinic- higher prevalence of vagal LAF (OR 5.06, 95% CI
ally significant cardiac arrhythmia in clinical prac- 1.35 to 19).12 Baldesberger et al13 published similar
tice. The prevalence of AF among men below data in a study of 62 professional cyclists who
40 years of age in the general population is 0.5%,1 completed the Tour de Suisse professional cycling
and increases to 8% in those above 80 years.2 race at least once during the years 1955–1975.
Several cardiac and non-cardiac conditions, includ- These cyclists were matched for age, weight,
ing age, structural heart disease, hypertension, dia- hypertension and cardiac medication with a
betes mellitus and hyperthyroidism,3 have been control group of 62 male golfers who had never
described as risk factors for developing AF. performed high-endurance training. The incidence
However, in a subset of patients with AF younger of AF and AFl was significantly higher among ath-
than 60 years, routine evaluation including phys- letes. Heidbuchel et al14 analysed the relationship
ical examination, laboratory tests including between a history of endurance sports activity
thyroid function, echocardiography and exercise and/or its continuation and the risk of developing
stress testing does not reveal any cardiovascular AF in patients with AFl undergoing right isthmus
disease or any other known causal factor. These ablation. Of the 137 patients included, 31 (23% of
patients are considered to suffer from ‘lone’ AF the whole population) were mainly engaged in
(LAF).4 The reported prevalence of LAF varies from endurance activities. A history of endurance sports
2% to 50%, depending on the chosen study popu- participation was an independent risk factor for
lation with AF.5 6 AF development after flutter ablation (multivariate
Although benefits of regular exercise on reduc- HR 1.81, 95% CI 1.10 to 2.98) and ongoing prac-
tion of the risks of cardiovascular diseases have tice of an endurance sport after AFl ablation also
been demonstrated,7 8 there is growing evidence increased the risk of AF (multivariate HR 1.68,
that long-term endurance exercise may increase 95% CI 0.92 to 3.06).
the risk of developing AF and atrial flutter (AFl) in In a further cohort study, we evaluated the inci-
middle-aged populations.9–17 dence of LAF in 183 individuals who ran the
This article discusses the prevalence of AF and AFl, Barcelona Marathon in 1992 in comparison to 290
pathophysiological mechanisms, clinical presentation sedentary healthy individuals. The incidence of
and treatment strategies in endurance athletes. LAF was higher among marathon runners com-
pared to sedentary men (annual incidence: 0.43/
AF AND ENDURANCE SPORT 100 for runners, 0.11/100 for sedentary men) at
Several studies have described a relationship 10 years of follow-up.15 In the GIRAFA (Grup
between long-term endurance sport practice and Integrat de Recerca en Fibril-lacio Auricular)
AF and AFl9–20 (table 1). In 1998, Karjalainen et al9 study,16 our group recruited patients with recent
concluded that vigorous long-term exercise is onset LAF attending the emergency room at our

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Table 1 Summary of the published studies analysing the relationship between atrial fibrillation and atrial flutter and endurance sport practice
Prevalence of
AF (%)
% (patients/
Studies Type of study Men Age (years) Type of sports Cases/controls controls) Relative risk for AF

Kaarjalainen Longitudinal case/ 100 47±5 runners Orienteering 262/373 5.3/0.9 5.5 (95% CI 1.3 to 24.4)
et al9 control (p=0.012)
49±5 controls
Mont et al10 Retrospective/ 100 44±13 sports Endurance sports 70 LAF 63/15 (p=0.05) N/R
compared to >3 h/week
general population 49±11
non-sports
Elosua et al12 Retrospective 100 41±13 AF Endurance sports 51/109 32/14 (p=0.01) 2.87 (95% CI 1.20 to 6.91)
case/control patients
44±11 Current practice
controls and >1500
cumulated hours of
practice
Heidbuchel Case/control in 83 53±9 sports
et al14 patients
undergoing flutter
ablation
60±10 Cycling, running 31/ 81/48 1.81 (1.10–2.98)
controls or swimming 106 (p<0.01)
>3 h/week
Molina et al15 Longitudinal case/ 100 39±9 runners Marathon running 252/305 5/0.7 8.80 (95% CI 1.2 to 61.2)
control (p=0.013)
50±13
sedentary
Baldesberger Longitudinal case/ 100 67±7 cyclist Cycling 134/62 10/0 (p=0.028)
et al13 control 66±6 golfers
Mont et al Prospective case/ 69 48±11 Endurance sports 107/107 N/R 7.31 (95% CI 2.33 to 22.9)
GIRAFA control
study16
Grimsmo Prospective 100 Group I, Cross-country Group I, 33; group II, 37; 12.8% of LAF Long PQ (rr=0.38, p=0.001
et al19 54–62; group skiers group III, 8 and rr=0.27, p=0.02),
II, 72–80; bradycardia (rr=0.29,
group III, 87– p=0.012) were associated risk
92 factors
Winhelm Retrospective 100 42±7 Running 70 cases, stratified according to 6.7% Signal-averaged P-wave
et al20 lifetime training hours: low-training duration (p=0.026), LA
group: <1500 h: 17 medium-training volume (p=0.001), vagal
group:1500–4500 h: 21 high-training activity (p=0.002), PAC
group:>4500 h: 22 (p=0.026) increased in high
training group.
LA, left atrial; PAC, premature atrial contractions.

hospital between January 2001 and June 2005. They were Prix of Bern, one of the most popular 10-mile races in
matched by age and sex with healthy controls. An association Switzerland, and found that the prevalence of AF was 6.7%.
of LAF and accumulated hours of physical activity was In contrast to these previous studies, Pelliccia et al21 analysed
described: intense physical activity of >564 h was associated the frequency of AF and supraventricular tachycardias in 1777
with a risk for developing AF of 7.31 (95% CI 2.33 to 22.96). highly trained athletes. They reported a low incidence of AF
A recent meta-analysis by Abdulla and Nielsen17 demon- among competitive athletes (0.2%), similar to that observed in
strated that the overall risk for AF was significantly higher in general populations of comparable age and sex. However, in
athletes than in controls (OR 5.29, 95% CI 3.57 to 7.85). contrast to previous studies showing an association between
Additionally, these results were confirmed by a large prospective AF and long-term endurance sport practice, the population
cohort study of apparently healthy men.18 After adjustment for analysed by Pelliccia et al comprised young athletes (mean age
multiple potentially confounding lifestyle factors and health 24±6 years) involved in vigorous training programmes for a
conditions, Aizer et al showed a 20% increased risk of develop- mean time period of only 6 years.
ing AF among individuals with higher frequency of participa- On the other hand, in the Cardiovascular Health Study,22
tion in a regular programme of vigorous exercise. More recently, the incidence of AF in older adults (>65 years old) was lower
Grimsmo et al19 analysed the prevalence of LAF in 117 cross- with moderate-intensity exercise. However, this was not true
country skiers who competed in the Norwegian ‘Birkebeiner’ with high-intensity exercise.
race of 58 km. They found that the prevalence of LAF was In summary, previous studies support an association between
approximately 13% and bradycardia and long PQ time were long-term endurance sports practice and the occurrence of
independent predictors for the occurrence of LAF. Winhelm arrhythmias such as AF or AFl in the middle-aged male
et al20 recruited non-elite athletes participating in The Grand population.

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AFL AND ENDURANCE SPORT ACTIVITY the occurrence of LAF. Winhelm et al20 showed that athletes in
Many of the described series report the presence of both AF the high training group (>4500 h of lifetime training) had a sig-
and AFl in endurance athletes. Hoogsteen et al11 found that AFl nificantly greater parasympathetic tone (figure 1). Therefore,
was present in 10% of athletes with paroxysmal AF. the increased vagal tone induced by endurance sport practice
Baldesberger et al13 evaluated arrhythmias in a long-term might explain the appearance of AF.
follow-up (30–50 years) after high endurance training in former
professional cyclists, and found that AFl was more common Exercise and structural changes in the atrium
than AF. It is well known that the athlete’s heart, although assumed to
Heidbuchel et al14 described a higher incidence of AF after be a physiological adaptation, has increased atrial size and ven-
common flutter ablation in endurance athletes than in controls. tricular mass and altered diastolic function, which may create a
According to these authors, flutter ablation could unmask the favourable substrate for the disease.
underlying atrial disease in endurance athletes, resulting in AF Frustaci et al30 analysed the structural changes in the atria of
development during follow-up. patients with LAF. They described the presence of inflamma-
Based on these findings, endurance sport may contribute to tory lymphonomonuclear infiltrates, compatible with myocar-
the development of both arrhythmias. ditis, non-inflammatory cardiomyopathic processes and patchy
fibrosis. However, in the literature data regarding the cardiac
PATHOPHYSIOLOGY OF AF AND AFL IN ENDURANCE histological and biochemical remodelling in endurance athletes
ATHLETES are scarce.
The pathophysiological mechanisms responsible for the
increased risk of AF in individuals who practice an endurance Fibrosis
sport remain speculative. Atrial ectopic beats, inflammatory Our group analysed the morphological changes in an experi-
changes, changes in electrolytes, atrial enlargement with dilata- mental study in male Wistar rats.31 A group of rats was condi-
tion and fibrosis and increased vagal tone and bradycardia, tioned to run vigorously for 4, 8 and 16 weeks and compared to
among others, have been proposed as mechanisms. time-matched sedentary rats that served as controls. At
16 weeks of training, exercise rats developed eccentric hyper-
trophy and diastolic dysfunction as well as atrial dilation with
Atrial ectopic beats collagen deposition at the atria and the right ventricle. An
Conflicting data exist regarding increased atrial ectopy with increase in mRNA and protein expression of a series of fibrotic
physical activity. It is accepted that pulmonary vein ectopy markers in the right ventricle and in both atria was found in
may be the trigger in episodes of paroxysmal AF.23 Since atrial exercise rats compared to sedentary rats.
ectopy has been shown to be increased as a consequence of A case-control study by Lindsay and Dunn32 analysed the
physical activity,20 24 it has been proposed that increased atrial presence of humoral markers of fibrosis in 45 veteran athletes
ectopy might also explain the increased risk of AF associated compared to sedentary subjects. Athletes showed an increase in
with sport practice. However, these findings were not sup- three collagen markers—plasma PICP, CITP, and TIMP-1—
ported by Baldesberger et al,13 they did not find an increased suggesting that long-term sport practice may provoke fibrosis as
incidence of atrial ectopy, despite increases in ventricular part of the hypertrophic process in veteran athletes.
ectopy in former professional cyclists. More recently, Breuckmann et al33 prospectively analysed the
myocardial distribution of late gadolinium enhancement with
Influence of the autonomic nervous system delayed-enhancement cardiac magnetic resonance imaging in
The role of the cardiac autonomic nervous system in the initi- 102 non-professional male marathon runners and in asymptom-
ation and maintenance of AF has been widely investigated.25–28 atic age-matched control subjects. A three times higher rate of
In an elegant study, Coumel29 analysed the influence of auto- myocardial damage was found among runners compared to the
nomic innervations in patients with frequent attacks of parox- sedentary control group (12% vs 4%; p=0.077). Similar findings
ysmal AF and AFl; they found that two opposite patterns and were reported by Wilson et al,34 who described a high preva-
mechanisms (vagal and sympathetic, which often interact) can lence (50%) of myocardial fibrosis in healthy, asymptomatic,
be identified. According to these studies, the vagal influences veteran, male lifelong athletes, compared to zero cases in age-
predominated in normal atria, and the formation of macroreen- matched veteran controls and young athletes.
trant circuits such as flutter might be explained by the shorten-
ing of the wavelength of the atrial impulse as a consequence of Myocardial injury
vagal stimulation. Diseased atria, however, were more depend- Several studies have demonstrated elevations in highly specific
ent on adrenergic influences, which favoured the formation of cardiac biomarkers (cardiac troponin T and I) after prolonged
microreentries and automatic and triggered activities. Vagal AF exercise, suggesting that strenuous physical exertion may result
was originally described as AF that (1) predominantly affects in myocardial injury.35–40 A recent meta-analysis by Shave
males between 30 and 50 years of age, (2) usually occurs at et al41 demonstrated that the incidence of post-exercise cTnT
night and rarely occurs between breakfast and lunch when the release in the population of athletes was approximately 47%.
sympathetic tone is high, (3) rarely occurs during exercise or The mechanisms responsible for post-exercise cTnT release and
emotional stress, (4) is frequently triggered during relaxation the kinetics of cTnT release after exercise are not clear, and
after stress and (5) is often preceded by bradycardia. whether postexercise cTnT release is related to microinjury of
Most of the available data support the association between the myocardium remains to be determined.
sport practice and LAF, implicating increased vagal tone as the
principal underlying mechanism. According to the GIRAFA Inflammation
study,16 vagal AF was the most common form of LAF: 70% of A few studies have found that excessive training may lead to
consecutive patients with LAF had vagal AF. Grimsmo et al19 tissue injury, which activates circulating monocytes, producing
found that bradycardia and long PQ time were predictors for large quantities of IL-1β and/or IL-6 and/or tumour necrosis

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Figure 1 Signal-averaged P-wave duration, left atrial volume, vagal activity (expressed as root of mean squared differences of successive
normal-to-normal intervals) and number of premature atrial contractions in 24 h stratified according to lifetime training hours ( p values for analysis of
variance). Reproduced with permission from Winhelm et al.20

factor-α and systemic inflammation.42 Additionally, several group and left atrial size was associated with LAF in endurance-
studies have related an increase in C-reactive protein (CRP) and trained athletes.
interleukins (ILs) in both paroxysmal and persistent AF.44–46 Similarly, an enlarged left atrium (atrial volume >29.0 ml/
Elevation of CRP and IL-6 might also contribute to generation m2) was present in 24% of runners in the low-training group
and perpetuation of AF, as evidenced by marked inflammatory (<1500 h of lifetime training), 40% of runners in the medium-
infiltrates, myocyte necrosis and fibrosis found in atrial biopsies training group (1500–4500 h) and 83% of runners in the high-
of patients with LAF.30 43–45 training group (>4500 h of lifetime training) ( p=0.001).20
Such observations suggest that sustained, intensive overtrain- In addition, experimental studies of our group31 observed a
ing could produce a chronic inflammatory response in athletes left atrial dilatation, left ventricular hypertrophy and dilatation
that increases their risk for AF. However, there are no studies in at 16 weeks of training, findings that are consistent with the
the literature that confirm the association between AF, inflam- features of the athlete’s heart described in humans.
mation and exercise. The reversibility of arrhythmogenic remodelling has also
been assessed. A few studies have reported reversal of the
remodelling associated with long-term exercise after long-term
Atrial remodelling
detraining.48 Our group evaluated whether a period of rest
Atrial remodelling has been shown to be present in elite ath-
could allow reversion of the profibrotic changes induced by
letes. Pelliccia et al21 reported that 20% of endurance sport ath-
endurance training.31 The abnormal cardiac remodelling caused
letes had larger left atrial dimensions compared to sedentary
by 16 weeks of intensive exercise were reversed after 8 weeks of
controls. Similarly, D’Andrea et al47 showed that LA enlarge-
detraining.
ment is relatively common in top-level athletes. GIRAFA study
The role of physical activity cessation and its effect upon AF
data16 showed that patients with LAF had a larger atrium than
will be further discussed in the text.
the controls. Furthermore, there were no differences in left
atrial size between patients with a first episode of AF and those
suffering recurrences, suggesting that structural changes were CLINICAL CHARACTERISTICS OF SPORT-RELATED AF
present before onset of AF. Grimsmo et al19 found that the left The usual clinical profile of sport-related AF is a middle-aged
atrial diameter and the left atrial area were larger in the AF male athlete, with a history of long-term regular endurance

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sport practice who is currently involved in regular, high- of AF, especially in patients with paroxysmal AF and no struc-
intensity endurance sport practice. tural heart disease.55 Recent data support the efficacy of abla-
AF typically presents as a paroxysmal and highly symptom- tion strategy in athletes. Furlanello et al56 described a 90%
atic crisis, initially very occasional and self-limited, but success after a mean of two ablation procedures in 20 athletes,
becomes more frequent and prolonged over the years and can with a significant improvement in all quality-of-life parameters
progress to persistent AF. Hoogsteen et al11 found that 17% and in particular in those pertinent to physical functioning.
exercise-related paroxysmal AF progressed to persistent AF and We compared the effectiveness of CPVA between a popula-
the GIRAFA study16 showed that 43% of patients with tion of endurance athletes (defined as those who performed
exercise-related AF were in persistent AF. Characteristically, AF regular endurance sport activity for at least 3 h per week for at
episodes occur at night or after meals, revealing that AF may be least the 10 years immediately preceding the arrhythmia diag-
related to increased vagal tone.16 The AF crisis frequently coex- nosis) with LAF and other patients with AF.57 There were no
ists with common AFl in many patients. differences in CPVA effectiveness between the two groups
(figure 2A). Furthermore, left atrial diameter and long-standing
MANAGEMENT OF AF IN ATHLETES AF, but not endurance sport practice, were the only independ-
A careful history of all the potential contributing factors should ent predictors of recurrence. More recently, Koopman et al58
be taken. Medical conditions such as hyperthyroidism, pericar-
ditis, Wolff-Parkinson-White syndrome, hypertrophic cardiomy-
opathy or long QT syndrome must be ruled out. Alcohol
consumption and other substances such as caffeine, anabolic
steroids, cocaine or sympathomimetics in cold medicines
should be investigated and discontinued.

Sport activity reduction

Furlanello et al48 described a good response to sport abstinence
in top-level athletes with AF. Similarly, Hoogsteen et al11
showed that up to 30% of athletes experienced fewer episodes
of AF by reducing sport activity. Therefore, the initial approach
should be to recommend reducing physical activity. According
to the Study Group on Sports Cardiology of the European
Association for Cardiovascular Prevention and Rehabilitation,49
athletes in an early stage of paroxysmal AF should discontinue
training for 2 months to stabilise sinus rhythm. The degree of
improvement during this resting period will determine whether
athletes are allowed to resume their training.
Task Force 7 of the 36th Bethesda Conference50 recommends
that athletes with asymptomatic AF in the absence of structural
heart disease can be permitted to participate in any competitive
sport, provided they 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.
Asymptomatic athletes who have AF episodes lasting 5–15 s
with no increase in duration during exercise can participate in all
sports. Athletes should take medications that slow down the ven-
tricular rate and should stop exercise training if there is a history
of high ventricular rate or haemodynamic instability during AF.
In these patients, we usually prescribe AV-node slowing agents
despite moderate bradycardia during sinus rhythm.

Pharmacological options
Class I antiarrhythmic drugs can be initiated for the prevention
of AF episodes once adequate ventricular rate control during
exercise has been assured. However, although these drugs may
prevent AF recurrences, AF can also be converted into AFl.51 52
Therefore, a combination with calcium channel blockers is
recommended.53 54
The ‘pill-in-the pocket’ approach with class I drugs is recom-
mended in athletes with paroxysmal AF. Sport activity should Figure 2 (A) Kaplan-Meier curves for long-term freedom from
recurrent arrhythmias after a single ablation procedure in lone atrial
be limited in these patients until at least one half-life of the
fibrillation athletes group (dashed line) and control group (solid line).
antiarrhythmic drug has passed.49 Reproduced with permission from Calvo et al.57 (B) Kaplan-Meier curves
for final outcome after multiple ablations, on or off drugs. AF, atrial
Pulmonary vein ablation fibrillation. p value: log-rank p for 5-year follow-up, endurance athletes
Circumferential pulmonary vein ablation (CPVA) has been versus non-endurance athletes versus controls. Reproduced with
introduced in clinical practice as an effective and safe treatment permission from Koopman et al.58

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analysed the efficacy and success rate of radiofrequency catheter Contributors Lluís Mont and Josep Brugada.
ablation for AF in an athlete population in comparison with Patient consent Obtained.
contemporary controls. Athletes were defined as those who per- Ethics approval Ethic Committee of Hospital Clínic of Barcelona.
formed sport for ≥3 h per week during ≥10 years or for a total
Provenance and peer review Commissioned; externally peer reviewed.
of ≥1500 h after the age of 14 years. Compared with the
control group, endurance and non-endurance athlete groups had
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