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European Journal of Echocardiography 2008 9(2):261-267; doi:10.1016/j.euje.2007.03.001
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Published on behalf of the European Society of Cardiology. All rights reserved. © The Author 2007. For permissions please email: journals.permissions@oxfordjournals.org

Echocardiographic findings in former professional cyclists after long-term deconditioning of more than 30 years

Pia Luthi1, Michel Zuber2, Manfred Ritter3, Erwin N. Oechslin4, Rolf Jenni4, Burkhardt Seifert5, Sylvette Baldesberger1 and Christine H. Attenhofer Jost1,*

1 Cardiovascular Center, Klinik Im Park, Zurich, Switzerland
2 Outpatient Clinic Othmarsingen, Zurich, Switzerland
3 HerzZentrum, Zurich, Switzerland
4 Cardiovascular Center, Clinic for Cardiology, University Hospital Zurich, Zurich, Switzerland
5 Department of Biostatistics, University of Zurich, Zurich, Switzerland

Received 29 July 2006; accepted after revision 4 March 2007; online publish-ahead-of-print 10 May 2007.

* Corresponding author: Cardiovascular Center Zurich, Klinik Im Park, Seestr. 220, 8027 Zurich, Switzerland. Tel: +41 44 209 2020; fax: +41 44 209 2029. E-mail address: ch.attenhofer{at}attglobal.net


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
Background: In professional cyclists, typical changes include reversible dilatation of atria and left ventricle (LV), LV hypertrophy but normal diastolic function. Data on long-term outcome are limited.

Methods: Of all 134 former Swiss professional cyclists (PC) participating ≥1x in the professional bicycle race Tour de Suisse from 1955 to 1975, 62 (42%) were recruited for a prospective case control study. The PC and a control group of 62 golfers (matched for age, gender, hypertension, present physical activity) were screened [clinical examination, history, echocardiography, measurement of proBNP (normal <227 pg/mL)].

Results: The interval since the last bicycle race as PC was 38 (15–49) years. Average age at exam was equal in controls and PC (66±6 vs 66±7 years; P = 0.73). Percentage of participants undergoing >4 h of endurance training per week was identical (P = 0.72). Total kilometers (km) on the bicycle were higher in PCs with 311,000 (60,000–975,000) than in controls (2500 [0–120,000]; P < 0.0001). PC had larger atrial volume indices (P = 0.002) and tended to have higher LV muscle mass indices (P = 0.07). Multiple regression analysis identified the total number of bicycle km as an independent factor for LV muscle mass. For left atrial size, heart rate at rest, age, years since the last bicycle race and the current hours of endurance training were identified as independent predictors. Long axis function of both ventricles (systolic velocities of mitral and tricuspid annulus) was decreased in PC (P ≤ 0.04). There were signs of diastolic dysfunction with lower annular E' and A' velocities. ProBNP levels were comparable in both groups (P = 0.21).

Conclusion: Among former PC, there seems to be incomplete cardiac remodelling with differences in systolic and diastolic function between former PCs and controls in the long time follow-up. Former high level endurance training may have a persisting impact on cardiac size and function.

Keywords: Athlete's heart; Cyclists; Systolic function; Diastolic function; Long axis function; Left ventricular muscle mass


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusions
 References
 
Long-term physical training is associated with an increase in left ventricular (LV) cavity dimension, wall thickness and mass resulting in an ‘athlete's heart’.1–3 The athlete's heart shows a balanced enlargement with similar changes in both ventricles.4 Two different forms of athlete's heart can be distinguished: concentric remodelling in athletes undergoing extreme weight lifting and eccentric remodelling in athletes undergoing endurance training.1,5 Cyclists and rowers have the largest LV cavity dimensions.6,7 Although in athletes, the resting ejection fraction is normal, systolic and diastolic left ventricular function is not impaired, which differs from hypertrophic cardiomyopathy or hypertensive heart disease.2 Brain natriuretic peptide (BNP) levels are only elevated in hypertensive participants but not athletes with increased LV mass index.8

Some suggest that long-term athletic training may result in left atrial enlargement which may not be totally reversible.9 While some studies showed no differences in cardiac function after deconditioning,10,11 others reported that there may be a partly irreversible LV hypertrophy with impaired LV diastolic filling especially if athletic training lasted for a long time.12 The potential for ventricular remodelling of the hearts in athletes is still subject of considerable debate. Ventricular hypertrophy as a physiological adaptation with no pathological consequences in athletes has been questioned.13

Therefore the goal of this study was to assess persistent echocardiographic changes many years after long-term high endurance training in former professional cyclists (PC). The echocardiographic findings and proBNP levels in these PC were compared to age- and gender-matched controls that had never performed high endurance competition.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusions
 References
 
Study group
All Swiss PC who participated at least once in the professional cycling race Tour-de-Suisse between 1955 and 1975 were included. Within this period, 134 Swiss cyclists have competed in the Tour-de-Suisse. Among these, 24 died (no death certificates available), 7 live abroad, 11 could not be traced, 29 refused participation, and 63 agreed to collaborate in the present study. Informed consent was obtained for each participant. One participant was not included because of the incidental finding of a tumour in the right ventricle, so there were 62 PC. The 62 male controls were selected among a group of senior golfers who had never performed competitive high endurance training. They were matched for age and body mass index.

Hours of calories expenditure were counted as follows: one hour of playing tennis, jogging, rowing, or riding the bicycle. The hours of playing golf were divided by four to account for the lower cardiovascular impact of playing golf (no electrical carts) in comparison to cycling or running. Exclusion criteria for golfers were previous high endurance exercise training, and severe congenital heart disease.

The examinations were performed between October 2004 and June 2005.

The research protocol was approved by the local ethics committee. Informed written consent was obtained for all subjects.

Echocardiography
A complete 2-dimensional and Doppler echocardiographic examination was performed in all participants according to the recommendations of the American Society of Echocardiography, including 2-dimensional guided M-mode measurements.14 A complete echocardiographic exam was feasible in all study participants. Left ventricular muscle mass index was calculated using the Devereux-modified American Society of Echocardiography cube equation using the left ventricular end diastolic diameter and the septal and posterior wall thickness.7,15 All examinations were stored in digital format and checked for correct measurements by an independent cardiologist. Left ventricular diastolic function was assessed as previously described by measuring the left ventricular inflow pattern at the tip of the mitral valve leaflets and the pulmonary venous flow pattern in the right lower (or upper) pulmonary vein.16,17 In all participants, Doppler tissue imaging was performed at the lateral mitral and tricuspid annulus. Using previously published criteria, diastolic function was graded as follows: normal, abnormal relaxation, or pseudonormal or restrictive pattern. Severe diastolic dysfunction was defined as a pseudonormal or restrictive filling pattern. Left ventricular biplane ejection fraction was measured by Simpson's method. A normal ejection fraction was defined as 50%–70%. Right ventricular diameter was measured at end-diastole in the apical 4 chamber view in the half distance between tricuspid annulus and apex. Size of right atrial area was measured at end-diastole in the 4-chamber view. Fractional area change of the right ventricle was measured as previously described.18 Longitudinal systolic function of both ventricles was assessed with the measurement of systolic velocities in the Doppler tissue imaging at the level of the lateral mitral and tricuspid annulus. From each measurement, the average of at least 3 measurements was averaged.

ProBNP and creatinine determination
For proBNP determination, an electro immunoassay of Roche was used. Normal values for proBNP levels are <227 pg/mL. ProBNP levels were taken at rest without previous exercise after 10 min in the supine position.

Serum creatinine was kinetically determined in the serum by using the alkaline picrate (Jaffe) method (Bayer). Normal values for men are 66–128 µmol/L.

Cardiovascular risk factors
Hypertension was defined as diastolic blood pressure of ≥90 mmHg, systolic blood pressure of ≥140 mmHg, or current medication for hypertension.Hyperlipidemia was defined as a cholesterol level of ≥5.2 mmol/L or HDL-cholesterol of <0.9 mmol/L. Subjects with a fasting plasma glucose level of 7.0 mmol/L and/or a 2-h plasma glucose level of 11.1 mmol/L during an oral glucose tolerance test and/or who were receiving antidiabetic medications were diagnosed with diabetes mellitus. Smoking was defined as current smoking or a history of habitual smoking. Positive family history for heart disease was defined as a first degree relative having known coronary artery disease at age <55 years for a male relative and <65 years for a female relative.

Statistics
Descriptive statistics include frequencies and percentages for categorical data, mean ± SD for approximately normally distributed data and median (range) for markedly non-normally distributed data. Fisher's exact test and Chi-square test were used to compare categorical data between PC and controls. The Mann–Whitney test was used to compare continuous data. Correlations between continuous variables were analysed using Spearman's rank correlation, all tests were applied two-tailed and a P-value of less than 0.05 was considered to be statistically significant. Stepwise regression analysis was performed including the variables: heart rate at rest, years since the last professional bicycle race, total bicycle distance and current hours of endurance training. Data were analysed using SPSS 11 (SPSS inc., Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusions
 References
 
The PC had been amateur competitive cyclists for 6 (range: 1–10) years and professional competitors for 4.5 (1–18) years resulting in an overall time of 10 (4–25) years as competitive cyclists. They had stopped their participation in professional cycling 38 (15–49) years ago. During the professional time they cycled 25,200 ± 9700 km/year maximally. Overall, they had performed 311,000 (60,000–975,000) bicycle km, compared to 2500 (0–120,000) bicycle km in the control group (P < 0.0001).

The clinical characteristics are shown in Table 1. Age and body mass index were comparable in both groups. Apart from smoking, there was no significant difference in cardiovascular risk factors, previous occurrence of heart failure, angina, myocardial infarction or dyspnea on exertion. The current hours of endurance training were only slightly higher in PC, and the percentage of study participants performing more than 4 h of endurance training was comparable in both groups. Sinus rhythm was present in 57 of the 62 PC and in all controls (P = 0.057). Five of the PC were in persistent atrial fibrillation or flutter. The heart rate at rest was slightly lower in PC (P = 0.008). There was no difference in cardiac medication including beta-blocker therapy, diuretics, ACE-inhibitors, angiotensin II receptor antagonists and calcium channel antagonists (P > 0.05).


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  		Table 1 Clinical baseline characteristics of the former professional cyclists and controls

 
Echocardiographic findings
A summary of the most pertinent echocardiographic findings is shown in Table 2. The PC had still a larger left ventricular size which is reflected in a slightly larger left ventricular end-diastolic diameter (P = 0.01) and left ventricular end-diastolic volume indices (P = 0.0009). However, in neither PC nor controls, left ventricular end-diastolic diameter was larger than 59 mm. In PC, left ventricular ejection fraction tended to be slightly lower than in controls (P = 0.09). There was no significant difference in the thickness of the interventricular septum; the left ventricular muscle mass tended to be slightly larger in PC (P = 0.07).


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  		Table 2 Echocardiographic findings of ventricular size, muscle mass and function

 
There was a significant difference in atrial size: both, right and left atria were considerably larger in PC than in controls. Exclusion of subjects with atrial fibrillation did not alter these findings. Also, the right ventricular diameter tended to be larger in PC (P = 0.048). A right ventricular end-diastolic diameter of more than 4.0 cm was present in 2 controls and 5 PC.

Peak systolic velocities of the lateral left and right ventricular annulus assessed by tissue Doppler imaging reflecting long-axis function was slightly lower in PC (P = 0.03 and P = 0.04, respectively).

There was no difference in estimated systolic pulmonary artery pressures: systolic pressure difference between the right ventricle and right atrium was comparable (21 ± 6 mmHg in 51 former PC vs 22 ± 4 in 39 controls in whom it could be measured).

Table 3 summarizes left ventricular diastolic function in subjects with sinus rhythm.


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  		Table 3 Diastolic function in former athletes and controls

 
E velocity and A duration tended to be lower in PC (P < 0.05) but there was no significant difference in E deceleration time, E/A-ratio and A-velocity. The results of tissue Doppler imaging showed considerably lower values of E'- and A' velocities of the left lateral ventricular annulus and of the A' velocity of the right lateral annulus in PC. Pulmonary venous systolic or diastolic flow and atrial reversal were similar in both groups. However, a larger difference in duration between mitral A wave and pulmonary vein A wave (pulmonary venous atrial reversal exceeding mitral A wave duration) was present indicating higher left ventricular end-diastolic filling pressures in PC (P = 0.02).

Former PC and controls could not be separated by assessment of diastolic function by the different categories; no restrictive filling pattern was present in any participant.

Creatinine and proBNP
The results of creatinine and proBNP measurements are shown in Table 4A and B. The prevalence of an elevated ProBNP level was only significantly higher in PC if the 5 former athletes with atrial flutter/fibrillation are included. Creatinine levels were significantly higher in the PC group, however with essentially identical mean values, suggesting no clinical difference.


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  		Table 4 Comparison of ProBNP and creatinine serum levels

 
Impact of number of total bicycle kilometers
In PC, the total number of bicycle kilometers had a moderate impact on left ventricular muscle mass index and atrial size (especially left atrial size). Figure 1 shows only a moderate correlation of left size with the total number of bicycle kilometres. The correlation was Rho = 0.40 (Spearman rank correlation, P = 0.002). There was a fair correlation between the left ventricular muscle mass index and the total number of bicycle kilometers of Rho = 0.53 (Spearman rank correlation, P = 0.0003, Figure 2). Independent risk factor analysis by step wise regression analysis assuming normal distribution of left ventricular muscle mass index showed the total number of bicycle kilometres was an independent risk factor for the left ventricular muscle mass index.


Figure 1
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  		Figure 1 Correlation (Spearman rank correlation) of atrial size and total number of bicycle kilometres in 62 former cyclists. Linear regression line is included for illustration.

 


Figure 2
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  		Figure 2 Correlation (Spearman rank correlation) of total number of bicycle kilometres with left ventricular muscle mass index in 62 former cyclists. Linear regression line is included for illustration.

 
For left atrial size, heart rate at rest, age, years since the last bicycle race and the current hours of endurance training were identified as independent predictors by multiple regression analysis. For left ventricular size (left ventricular volume index), years since the last bicycle race were not an independent predictor by multiple regression analysis. Only the current hours of endurance training were an independent predictor for left ventricular size by multiple regression analysis.

In Figure 3, a typical example is shown of the former PC with most previous bicycle km (975,000) and normal blood pressure throughout his life. He has left ventricular hypertrophy, impressively dilated atria despite the fact that he now performs only 2 h of mild endurance training per week due to dyspnea on exertion NYHA II–III.


Figure 3
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  		Figure 3 Example of an 86 year old former professional cyclist with 975 previous bicycle years. This shows the apical 4 chamber view of this participant. He still performs 2 h of endurance training per week. He had no cardiovascular risk factors including normal blood pressure. The left ventricular end-diastolic diameter is 52 mm, the left ventricular muscle mass index 146 g/m2 body surface are, the left ventricular ejection fraction 69%. Left atrial volume index is 83 mL/m2 body surface area. He received a pacemaker due to bradycardic atrial flutter. He has shortness of breath NYHA II and had intercurrent symptoms of heart failure. LA = left atrium; RA = right atrium; LV = left ventricle; RV = right ventricle.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusions
 References
 
Our results show that cardiac remodelling is not completely reversible in professional cyclists even after a very long follow up. Persistent changes compared to controls include dilated atria, changes in diastolic function and systolic function reflected as decreased long-axis function and in some subjects increased levels in proBNP. Atrial volume and LVMMI correlate with the extent of previous bicycling performed assessed by distance in kilometres on the bicycle. Cardiac changes in extreme endurance athletes may thus not be as physiological and benign as previously presumed.

Left ventricular size, muscle mass and systolic function of both ventricles
Left ventricular remodelling in PC has been described in many studies with an increase in both cavity size and wall thickening due to a combination of volume and pressure overload.1 The largest dimension of a LV diameter (73 mm) ever reported was measured 1998 in a cyclist who took part in the cycling race Tour de France.7 However, this is rare and might also have been due to underlying heart disease especially as it was associated with wall thinning.7 In elite athletes, LV enlargement of >60 mm has been described to occur in 14–51%,7,19 respectively, if corrected for body surface area of up to 35%,7 but very long time follow up studies of these subjects comparable to our study have not published to our knowledge.

None of our PC had persistent LV dilatation of more than 59 mm in the long time follow up which indicates almost complete morphologic remodelling of LV in our study group. This is consistent with several publications that described regression of left ventricular changes taking place within several weeks.20–22 However, left ventricular mass index in the PC of Abergel's study with reversible changes (was 144 ± 23 g/m2)7 compared to our former PC in whom 38 ± 7 years after their competitive races, left ventricular muscle mass index had regressed to 110 ± 32 g/m2 body surface area. Left ventricular ejection fraction is comparable to the active PC of Abergel with 61 ± 6% in 1998 and 62 ± 8% in our study group.7 However, there are no publications reporting the longitudinal function of the left and right ventricle in follow-up studies in former athletes. Reduced annular systolic velocities by tissue Doppler imaging are reflecting reduced long-axis function which is the most sensitive marker for disease. In our study tissue, decreased long-axis function in former PC may indicate persistent alterations of systolic function of both ventricles even in the very long time follow-up.

There have been reports describing right ventricular changes in active athletes (80% cyclists) with morphologic alterations in 47% by magnetic resonance imaging and 11% by echocardiography.23 Five of our former 62 PC had an enlarged right ventricle (8%) by echocardiography. Thus, changes in the athlete's heart involve both ventricles in both active and former high endurance athletes.

Atrial size and diastolic function
In our study, the difference in atrial size between the PC and controls, even after exclusion of PC with atrial fibrillation/flutter was impressive. In the literature, data on atrial size are scarce. It has been reported that atrial size is increased in competitive cyclists but diastolic function remains normal.24 Another study reported enlarged left atrial dimension in former endurance athletes at a mean age of 66 years in former cross country runners and skiers.9 However, this has not been related to diastolic dysfunction. Although, diastolic function was reported to be usually normal, there are some reports about lower A waves than E waves.2,22 Our data contradict the common assumption that diastolic function remains normal in former high endurance athletes as atria were larger and there is decreased E' velocity of the lateral annulus and shorter A duration of the left ventricular inflow. This may reflect that left ventricular, functional (in contrast to morphologic) remodelling of the hypertrophied ventricle of the active athletes is not physiological. Since atrial size is probably the best reflector of diastolic function, we therefore hypothesize that persistent dilatation of atria in former athletes also reflects persisting diastolic dysfunction.

Current endurance training is an independent predictor of left atrial and left ventricular size by multivariable analysis. However, even in former athletes not performing any endurance training, signs of functional remodelling can be impressive.

Correlation of cardiac changes with proBNP levels
It has been reported that BNP levels are related to left ventricular mass in hypertensive patients but not in cycling athletes.8 It was suggested that increased BNP levels in athletes may be a signal of coexisting pathology.8 However, proBNP levels were not elevated in our PC group and reflected normal filling pressure despite diastolic dysfunction. Only in those patients with atrial flutter/fibrillation proBNP levels were elevated. Our proBNP levels were taken in the supine position in the resting participant only. It has recently been reported that NT-proBNP levels can increase considerably from 28 ± 21 to 278 ± 152 ng/L immediately after a bicycle race (P < 0.001) in recreational cyclists.23

Impact of duration and extent of cycling
Our PC were a group of cyclists who performed intensive exercise and competitive cycling over many years (10 [4–25] years). If professional cycling should cause irreversible cardiac damage, then it should be related to length and extent of bicycling. In our study group, the total number of bicycle kilometres correlated fairly with atrial size and left ventricular muscle mass indicating that duration and level of exercise does have a long-term impact on ventricular remodelling and that irreversible changes may be prevented by limiting both time and extent of bicycling.

Limitations
Our study sample of 62 PC consisted of only 46% of all Swiss PC who participated in the Tour de Suisse during the study period 1955–1975. However, if PCs had died already (n = 24) or were too ill to participate in this study, an underestimation of the long-term impact on ventricular remodelling is even less likely than an overestimation.

Another limitation of the study is that maximal oxygen uptake VO2 has not been measured which would make the comparison between PCs and controls more valid.

Although the former PC perform slightly more endurance training than the controls, that small difference can not explain the observed differences between both groups. Moreover, most studies were performed between December to April when both groups did less endurance training due to poor weather conditions. There are seasonal variations in cardiac structure and function in cyclists: in the competitive season.24

We do not know the impact of performance-enhancing drugs in our former athletes. However, their active time of competition was from 1955 to 1975 when athletes had no access to growth hormones, erythropoietins, insulin etc. Doping usage at that time was mostly limited to wine and amphetamines. We can not definitely exclude that a mild catecholamine induced cardiomyopathy which can result in mild increases in left ventricular dimensions may have impacted the findings.

It could be argued that cyclists have an abnormal or supranormal heart to start with; however, no study has so far shown that competitive cyclists or other endurance athletes start with a larger heart prior to any endurance training.


   Conclusions
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
References
 
Among former PC, complete reversibility of exercise induced cardiac changes is not always present which makes the term ‘physiologic exercise induced changes’ inaccurate. Significant differences in systolic and diastolic function are found between former PCs and controls in the long-term follow-up. The extent of previous cycling correlates with left atrial size and left ventricular muscle mass index. Former endurance level training at an extremely high level and performed for many years may have a persisting impact on cardiac remodelling and function; if this has an impact on long-term poor outcome, it has yet to be shown.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 

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