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Cardiovascular diseases in Paralympic athletes
  1. Antonio Pelliccia1,
  2. Filippo M Quattrini1,
  3. Maria Rosaria Squeo1,
  4. Stefano Caselli1,
  5. Franco Culasso2,
  6. Mark S Link3,
  7. Antonio Spataro1,
  8. Marco Bernardi2,4
  1. 1Institute of Sport Medicine and Science, Rome, Italy
  2. 2Department of Human Physiology and Pharmacology, University Sapienza, Rome, Italy
  3. 3TUFTS Medical Center, Boston, Massachusetts, USA
  4. 4Italian Paralympic Committee, Rome, Italy
  1. Correspondence to Dr Antonio Pelliccia, Institute of Sport Medicine and Science, Largo Piero Gabrielli 1, Rome 00197, Italy; antonio.pelliccia{at}coni.it

Abstract

Background Sport participation (SP) of individuals with impairments has recently grown exponentially. Scarce scientific data, however, exist regarding cardiovascular (CV) risk associated with competitive SP.

Objective Assessing the prevalence of CV abnormalities and the risk for SP in Paralympic athletes (PA).

Methods PA (n=267; 76% men), aged 35±9 years, engaged in 18 sport disciplines, with a spectrum of lesions including: spinal cord injury (paraplegia and spina bifida) (n=116); amputation, poliomyelitis, cerebral palsy and other neuromuscular and/or skeletal disorders (Les autres) or visual impairment (n=151) entered the study. CV evaluation included history, PE, 12-lead and exercise ECG, echocardiography. Of these, 105 participated in ≥2 consecutive games, and had evaluations available over a 6±4 year follow-up.

Results Structural CV abnormalities were identified in 33 athletes (12%), including arrhythmogenic cardiomyopathies in 3, aortic root dilation in 3, valvular diseases in 7 (mitral valve prolapse in 4, bicuspid aortic valve in 3) and systemic hypertension in 11 (4%). In addition, ventricular (polymorphic, couplets or non-sustained ventricular tachycardia) or supraventricular tachyarrhythmias (atrial flutter, paroxysmal atrial fibrillation or SVT) were identified in 9 others. Over a 6-year follow-up, 6 of the 105 athletes (6%) developed CV diseases, including dilated cardiomyopathy in 1 and systemic hypertension in 5.

Conclusions PA present an unexpected high prevalence of CV abnormalities (12%), including a non-trivial proportion of diseases at risk for sudden death (2%), such as arrhythmogenic cardiomyopathies and dilated aortic root. This observation suggests that tailored recommendations for preparticipation screening and safe SP in this special athletic population are timely and appropriate.

  • Disabled
  • Athlete
  • Heart disease

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Introduction

Attention to individuals with musculoskeletal disabilities, which comprise a relatively small but important subset of global population, has been increasing in the past decade, with several legislative and societal initiatives promoted to restore their ability for full participation in daily work and leisure-time activities.1 Consequently, exercise programmes and dedicated sport events have seen increasing participation by individuals with disabilities. Participation in competitive and high-intensity sport activities has been growing exponentially in more recent times and, as a mere example, in the 2012 London Paralympic Games the record was attained of 4237 registered Paralympic athletes, competing in 20 different types of events and globally followed by 3.8 billion TV audience spectators.2

The astonishing performances that Paralympic athletes achieve have also raised a novel scientific interest, and prompted the issue of proper medical care of this unique athletic population. So far, very few studies, usually restricted to small groups of athletes, have addressed this topic and have reported conflicting functional or clinical features in Paralympic athletes.3–6

In this study we sought to assess the prevalence and type of cardiovascular (CV) abnormalities in this athletic population and the risk, if any, inherent to competitive sport participation. To address these objectives, we took advantage of a date set derived from a large cohort of Paralympic athletes, engaged in a broad spectrum of sport disciplines, evaluated in our medical programme before their participation in Paralympic Games.7 ,8

Methods

Study population

The Institute of Sports Medicine and Science, a division of the Italian National Olympic Committee, is responsible for the medical evaluation of elite Italian athletes, from which participants to either Olympic or Paralympic Games are selected. The medical programme routinely includes CV evaluation with history, physical examination, 12-lead resting and adapted exercise electrocardiography and echocardiography.8

For the purpose of this study, we considered all athletes evaluated for the Paralympic Games in the period from 2000 to 2012. The final study group included 267 athletes, 203 men (76%), aged 35±9 years (range 15–61 years, median 35 years). These athletes had achieved recognition in international events, including World Championships, and were chosen as participants to the Paralympic Games on the basis of their best performances.

Athletes included in the study population presented a variety of lesions, comprising those in wheelchairs with spinal cord injury (SCI), including individuals with paraplegia and spina bifida (n=116, or 43%); standing athletes, including individuals with visual impairment, amputation, poliomyelitis, cerebral palsy and with other musculoskeletal and/or neurological disorders called ‘les autres’ (n=151, or 57%).9

Athletes participated in a spectrum of 18 sport disciplines, arbitrarily defined as: (1) skill, including table tennis, equestrian, shooting, archery, curling and sailing (n=67; 25%); (2) power, including javelin, shot putting, short-distance running (100–200 m), alpine skiing and judo (n=56; 21%); (3) mixed, including basketball, ice-sledge hockey, tennis, fencing (n=64; 24%); and (4) endurance, including rowing, swimming, cycling, hand-bike, long-distance and marathon running and cross-country skiing (n=80; 30%).10

Written informed consent was waived for all athletes undergoing a standard clinical evaluation pursuant to Italian law and the Institute policy. The study design was approved by the Review Board of the Institute and funded by the Italian Paralympic Committee. All clinical data assembled on these athletes are maintained in an institutional database.

Electrocardiography

Standard 12-lead ECGs were performed with the subject in supine position after at least 3 min of rest, and recorded at 25 mm/s. ECG analysis was performed according to the most recent the ‘Seattle criteria’.11

Exercise testing

The exercise testing in wheelchair and standing Paralympic athletes with lower limb impairment was performed with arm-crank ergometer (Ergoline 800, Ergoline GmbH, Bitz, Germany). After a 3 min warm up at a constant power (30–50 Watts, according to body weight), the exercise was performed with a 10 watt increment of every minute until exhaustion.7 In athletes with visual or upper limb impairment, exercise testing was performed on a bicycle ergometer (Ergoselect, Cosmed, Italy), according to the same protocol, and pursued until exhaustion. Continuous ECG monitoring and recording were utilised during the exercise and subsequent 7 min recovery period.

Duplicate measurement of the blood pressure by sphygmomanometer was performed with the participant sitting in a quiet environment after 5 min of rest. Blood pressure during exercise testing was measured at baseline, peak exercise and after 5 min of recovery.

Echocardiography

Two-dimensional (2D) Doppler echocardiography was performed with Philips Sonos ie33 (Philips Medical System, Bothell, Washington, USA). Cardiac images were obtained in multiple cross-sectional planes using standard transducer positions. M-mode echocardiograms were derived from 2D images under direct anatomic visualisation. Measurements of end-diastolic and end-systolic left ventricular (LV) cavity dimensions, anterior ventricular septal and posterior free wall thicknesses were obtained as recommended by the American Society of Echocardiography.12 LV mass was calculated using the formula proposed by Devereux13 and was indexed to body surface area (BSA).

Ejection fraction was assessed in the apical four-chamber view and quantified according to modified Simpson's rule.12 Parameters of LV filling and relaxation were obtained with pulsed Doppler and TDI echocardiography, as described recently.14

Additional testing

The 24-hour ambulatory ECG monitoring was performed in athletes presenting with either ventricular ectopic beats (VEBs) at 12-lead ECG and/or at exercise testing, and/or with a history of potentially arrhythmogenic cardiac disease.15 Imaging tests, including cardiovascular MR (CMR; n=8) and CT (CT; n=2) scans were selectively performed in athletes when indicated to confirm diagnosis and to assess risk stratification. Electrophysiological studies (n=2) and radiofrequency catheter ablation (n=1) were performed in athletes with a history of recurrent palpitations and electrocardiographic evidence of atrial tachyarrhythmias.

Clinical follow-up

Of the overall population included in this analysis, a subset of 105 athletes participated in two or more consecutive Paralympic Games, and had serial evaluations at our Institute. Clinical, electrocardiographic and echocardiographic data of these athletes were available over a follow-up period of 1–16 years (mean 6±4).

Statistical analysis

Data are expressed as mean±SD. Comparisons between categorical and continuous variables were evaluated with χ2 test and Student's t test. A two-tailed p value <0.05 was considered statistically significant.

Results

Demographic and clinical characteristics

Mean age was 36±9 years (range 15–61) in men and 34±10 (range 16–55) in women (p=0.34). Body surface area was 1.87±0.18 (1.4–2.6 m2) in men and 1.61±0.2 (1.3–2.0 m2) in women (p<0.001). Systolic and diastolic blood pressures were higher in men as compared with women (124±11 vs 115±9 mm Hg; 80±7 vs 73±8 mm Hg, respectively; p<0.001). Resting heart rate was similar (66±13 in men vs 68±11 bpm in women; p=0.4).

When considered with regard to disability, there were no differences in athletes with regard to gender distribution, or mean age and body size. Heart rate was slightly higher in athletes using wheelchairs than in other athletes (70±11 vs 60±10 and 66±13 bpm; p<0.001), and blood pressure was mildly lower in athletes with visual impairments (119±10/78±8 vs 122±11/77±9 and 122±11/78±8 mm Hg; p<0.02).

When considered with regard to sport, athletes engaged in skill activities were relatively older compared with the remaining ones (39±9 vs32±6, 35±7 and 34±10 years; p<0.005). No differences were observed for gender distribution, body size or blood pressure. Heart rate was mildly higher in athletes participating in skill than mixed and endurance disciplines (75±12 vs 67±11 and 61±12 bpm; p<0.005).

Cardiovascular disorders

Structural CV abnormalities were identified in 24 athletes (9%) and major supraventricular or ventricular tachyarrhythmias (in the absence of structural cardiac abnormalities) in 9 (3%). The overall prevalence of CV disorders in the Paralympic athletic population was 12% (ie, 33/267) (figure 1, table 1).

Table 1

Cardiovascular abnormalities detected at the preparticipation screening programme for Paralympic athletes

Figure 1

Paralympic athletes. BAV, bicuspid aortic valve; CV, cardiovascular; DCM, dilated cardiomyopathy; MVP, mitral valve prolapse; RF ablation, radio frequency ablation; SV, supraventricular.

Arrhythmogenic cardiomyopathies were identified in 3 athletes (1%). Specifically, dilated cardiomyopathy was diagnosed in a 38-year visually impaired skier and 52-year archer with sciatic popliteal traumatic nerve lesion.16 None reported cardiac symptoms and physical examination showed the third heart sound in one. On echocardiography, the LV cavity was enlarged (ie, 56 and 62 mm, respectively), with impaired systolic function (ejection fraction, 40% and 45%), segmental wall thinning and evidence (in one) of intramural late gadolinium enhancement on CMR. In association, frequent and complex ventricular ectopic beats (VEBs) were recorded on 24-hour ECG monitoring in both athletes.

Hypertrophic cardiomyopathy (HCM) was identified in a yachter who was paraplegic.17 The athlete denied cardiac symptoms or performance impairment. An ejection murmur was present along the LV outflow tract. The 12-lead ECG showed inverted T-waves in inferior and lateral leads, and the echocardiography showed asymmetric LV hypertrophy (maximum wall thickness, 22 mm), systolic anterior motion of the mitral valve with mild outflow gradient (30 mm Hg, at rest) and dilated left atrium (transverse diameter, 53 mm). The 24-hour ECG monitoring showed polymorphic VEBs and a short nocturnal run of atrial fibrillation.

Isolated dilation of the aortic root (ie, ≥40 mm)18 was discovered on echocardiography in 3 (1%) athletes. A 45-year, asymptomatic, curler with paraplegia showed a marked dilation of the aortic root extending to the ascending aorta (maximum 52 mm), associated with mild regurgitation, with a tricuspid aortic valve. The remaining two athletes showed milder aortic root enlargement (ie, 41 and 42 mm), extending to the ascending aorta (37 and 38 mm, respectively). Physical examination was unremarkable in both.

Valvular diseases were found in 7 (3%), including mitral valve prolapse (MVP)19 in 4 (with mild regurgitation in one), and bicuspid aortic valve (BAV)20 in 3 (with mild regurgitation in two). Systolic murmur was audible in 3 (of the 4) with MVP and in 2 (of 3) athletes with BAV. Two athletes with MVP also had ventricular or supraventricular ectopic beats on 24-hour ECG monitoring, and one showed a borderline blood pressure profile.

Systemic hypertension (ie, blood pressure >140/90 mm Hg on repeated measurements, or current drug treatment)21 was present in 11 (4%) athletes. Of these, eight had a positive family history for hypertension, and eight showed either electrocardiographic and/or echocardiographic changes consistent with hypertensive cardiac disease.

In addition, supraventricular or ventricular tachyarrhythmias were recorded in 25 athletes, consisting of isolated and rare VEBs, in the absence of detectable cardiac abnormalities at imaging tests. However, nine of these athletes presented major tachyarrhythmias. Specifically, atrial flutter was recorded in a cyclist, and a paroxysmal burst of atrial fibrillation in a swimmer, both reporting of palpitations. Short runs of supraventricular tachyarrhythmia (ie, atrial-ventricular nodal re-entry tachycardia, AVNRT) were recorded in a rower and sledge hockey players, respectively, who denied symptoms. Finally, five other athletes presented frequent (>3000/24 hour) and/or polymorphic VEBs with couplets and/or short run of non-sustained ventricular tachycardia (NSVT). None referred cardiac symptoms and/or impairment in athletic performance.

Among the 33 athletes identified with CV abnormalities, primary suspicion for diagnosis was prompted by history and physical examination in 18 (55%, including palpitations in 2, hypertension in 11 and valvular diseases in 5), by addition of 12-lead ECG in 12 (36%, comprising supraventricular or ventricular arrhythmias in 7, cardiomyopathies in 3 and dilated aorta in 2), and by echocardiogram in 3 (9%, with valvular diseases in 2 and dilated aortic root in 1).

Clinical management and sport participation

Clinical management and sport participation was advised based on the current recommendations,22 ,23 and tailored to the Paralympic athlete's CV abnormality. Specifically, athletes with dilated cardiomyopathies and HCM received detailed information explaining the clinical presentation and outcome of their disease; were advised regarding tailored β-blocker treatment; and were restricted from Paralympic Games participation.

The curler with markedly dilated aortic root underwent surgical repair, with prosthetic aortic tube implanted. After 6 months of surgery, the athlete resumed training and competition. The two other athletes with mild aortic root enlargement entered a serial imaging follow-up, without further restriction.

Athletes with systemic hypertension had both nutritional and pharmacological treatment advised, and pursued competitive sport with periodical clinical follow-up. Athletes with valvular diseases entered a clinical and imaging follow-up, without restriction from sport participation.

An athlete with atrial flutter underwent successful radiofrequency ablation and after 4 weeks resumed training and competition. Athletes with complex/frequent ventricular arrhythmias, after imaging test excluded structural CV abnormalities, entered a clinical follow-up programme (with 6-month controls) without restriction from competitive sport.

Clinical changes over the follow-up

Of the 105 athletes evaluated during the 6±4 year follow-up period, 6 showed a new incidence of cardiac diseases. Specifically, dilated cardiomyopathy was identified in an amputee, sledge-hockey athlete at the age of 47 years, after a 10-year follow-up. The athlete denied symptoms or impairment in physical performance. Diagnosis was based on progressive LV cavity dilation (diastolic diameter increased from 56 to 62 mm), with apical thinning, and decreased ejection fraction (from 55% to 40%). In addition, ventricular tachyarrhythmias (up to 2000 VEBs/24 hour, with couplets, and a short run of NSVT) were found. The athlete was withdrawn from competitive sport participation.

Five other athletes developed systemic hypertension, associated in one with progressive enlargement of the ascending aorta (38–41 mm), and in another with occurrence of palpitations (identified as supraventricular tachycardia), which was successfully abolished by radiofrequency ablation. Treatment was advised and all entered a clinical follow-up.

Other findings

All Paralympic athletes included in the study population underwent mandatory antidoping controls.24 Over the 6-year period of observation, two athletes were found positive for banned drugs, including a 33-year-old, amputee male sprinter (200 m) (stanozolol) and a 30-year-old, amputee cyclist (fenoterol), who were disqualified from Paralympic competitions according to the World Anti-Doping Agency (WADA) rules.25

Discussion

Cardiovascular abnormalities in Paralympic athletes

The main finding of the present investigation was the unexpected high prevalence of CV abnormalities identified by our medical programme in elite Paralympic athletes. In this cohort, the prevalence of structural cardiac anomalies and major tachyarrhythmias was 12%, which largely exceeds the 1–2% we previously reported in Olympic athletes,26 and the 2% observed in amateur normal athletes entering the Italian national screening programme.27 The observed prevalence of CV disorders was particularly surprising, in consideration that the Paralympic athletes had been previously evaluated at the local level within the national preparticipation screening, before entering our programme for elite athletes.

We assume that certain characteristics of our Paralympic athletes may partially explain such a large occurrence of CV abnormalities, including their relative older age, and the diffuse presence of CV risk factors, as commonly observed in individuals with disabilities.28–30 This point is exemplified by the proportion of Paralympic athletes affected by systemic hypertension (ie, 4%), higher than we observe in relatively young, able-bodied Olympic athletes (ie, ≤2%). Similarly, Filho et al5 found an 11% prevalence of hypertension in 79 consecutive Brazilian Paralympic athletes. Nevertheless, we were surprised by the spectrum and the severity of cardiac disorders identified, which comprised a small, but not negligible proportion of CV diseases, such as arrhythmogenic cardiomyopathies (1%), or marked aortic dilation (1%), that is, conditions considered at risk for adverse events in association with competitive sport participation.22 ,23

Our observations clearly show that attaining a high level of performance, such as that required for participation in Paralympic Games, does not represent, per se, proof of absence of underlying cardiac disease. Indeed, most of the athletes identified with the most concerning cardiac disorders, such as arrhythmogenic cardiomyopathies, markedly dilated aortic root or even complex ventricular arrhythmias, denied symptoms or impairment in their physical performance and were among the best competitors in their sport discipline. Therefore, identification of the athletes at risk was possible only by our tailored preparticipation medical programme.

A relevant proportion (55%) of CV abnormalities was already suspected or identified by history and physical examination (due to the large proportion of hypertensive athletes), but the addition of the ECG increased the proportion of a vast majority (91%) of the CV disorders identified. We believe, however, that the imaging techniques (primarily echocardiography) had a major role in confirming the final diagnosis or assessing risk stratification, especially in athletes with cardiomyopathies and aortic diseases.

The large and unexpected proportion of cardiac disease identified in this Paralympic cohort raises medical and scientific concerns. We believe that our data clearly support the view that preparticipation evaluation for the CV disease represents an appropriate strategy to identify timely individuals with treatable cardiac disorders. Although divergent opinions currently exist regarding the feasibility and modalities of CV screening in young competitive athletes,31 ,32 our experience supports the concept that Paralympic athletes represent a distinct athletic population, with higher prevalence of CV disorders than previously supposed, and deserve specifically tailored medical care.

Another consideration that arises from our experience is the lack, at present time, of specific recommendations for evaluation and sport participation of individuals with disabilities who have CV diseases. Different from the plethora of papers related to able-bodied athletes,22 ,23 no focused documents have so far been released on this topic by the sport governing bodies or scientific societies. We believe that our findings demonstrate the urgency to discuss appropriate recommendations specifically tailored for Paralympic athletes, which appear to be the most fragile cohort among all athlete populations.

One more reason of concern arises from the antidoping programme, which testifies that a small, but a non-trivial proportion of Paralympic athletes were exposed to the harmful effects of banned drugs. From a cardiologist's perspective, this observation claims for a more vigilant attention of the poorly known CV effects of the banned drugs in this athletic population.

In conclusion, this study demonstrates an unexpected large prevalence of CV disorders in Paralympic athletes, including a small but important proportion of cardiac conditions at risk, such as arrhythmogenic cardiomyopathies, dilated aortic root and complex ventricular tachyarrhythmias. This observation suggests that recommendations for screening modalities and advices for competitive sport participation tailored to Paralympic athletes are timely and appropriate.

What are the findings?

  • Paralympic athletes are engaged in intensive training and demanding competitive events, despite a varied type and extent of disability. Their outstanding performances are often misjudged as evidence for lack of serious cardiovascular (CV) conditions. This study demonstrates for the first time a higher than expected prevalence of CV disorders, including a small but not negligible subset of cardiac disease at risk of acute events (such as cardiomyopathies or dilated aorta), in a large population of highly trained Paralympic athletes undergoing CV evaluation before participation in the Paralympic Games.

How might it impact clinical practice in the future?

  • Paralympic athletes represent a special segment of the athletic population, potentially exposed to a high CV risk, due to the presence of underlying, often undetected, cardiac diseases. Medical programmes to assess the presence of CV abnormalities and appropriate advice for competitive sport participation tailored to Paralympic athletes are timely and appropriate.

References

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Footnotes

  • Competing interests None declared.

  • Ethics approval Review Board of Institute of Sport Medicine and Science of Italian National Olympic Committee.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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