LE

Sports Medicine 13 (4): 270-284, 1992 0112.1642 /92 /0004-0270/$07.50/0 to Adis International Limited . All rights reserved. SP01110

Echocardiographic Findings in Strength- and Endurance-Trained Athletes Axel Urhausen and Wilfried Kindermann Institute of Sports and Performance Medicine, University of Saarland, Saarbrucken, Federal Republic of Germany

Contents Summary I. Echocardiographic Findings in Endurance-Trained Athletes I.I Total Heart Volume in Different Sports 1.2 Differentiation Between Pathologically and Physiologically Enlarged Hearts 1.3 Left Ventricular Measurements and Problematical Findings 1.4 Short Term Left Ventricular Adaptations to Endurance Training I.S Systolic and Diastolic Left Ventricular Function 2. Echocardiographic Findings in Strength-Trained Athletes 2.1 Influence of Body Dimensions 2.2 Left Ventricular Measurements and Problematical Findings 2.3 Systolic and Diastolic Left Ventricular Function 2.4 Influence of Anabolic Steroids on the Myocardium 3. Future Research 4. Conclusions

Summary

Assessment of echocardiographic measurements in athletes should take into account the specific sport and the quantity and quality of training. In addition, values corrected for body dimensions, especially the active body mass, should be used rather than absolute values. All parts of the athlete's heart are enlarged and its performance increases. Highly trained endurance athletes show the most enlarged hearts. Athlete's heart can be observed in athletes of all ages including the young. However, it is rarer than generally assumed . To differentiate between physiological and pathological myocardial changes, the relationship between heart size and ergometric performance as well as the echocardiograph ically measured ratio between left ventricular (LV) myocardial thickness and volume are useful; the latter remains unchanged, on the whole, in endurance- and strength-trained athletes . Concentric hypertrophy cannot be induced by strength training alone; additional factors, such as hypertension , aortic stenosis, cardiomyopathy or anabolic steroid use can play an important role. When corrected for body dimensions, non-endurance-trained, e.g. strength-trained, athletes have standard heart sizes even if considerable time is devoted to training . Findings in healthy untrained persons with large body dimensions also indicate no significant difference between the increase ofechocardiographic measures caused by training and that caused by growth. An LV myocardial thickness of 13mm is seldom exceeded even in the highly endurance-trained or anabolic drug-free strength trained athletes under physiological conditions. How-

Echocardiographic Findings in Athletes

271

ever, the echocardiographic differentiation of cardiomyopathy can be difficult if an individual is highly trained and has large body dimensions. In such cases, LV end-diastolic diameter may be up to 66 to 70mm. The upper normal value of LV muscle mass is 170 gfm2 for a physiological heart enlargement. Future areas of investigation should include: adaptative changes; of the right ventricle; differences in the regression of the athlete's heart after cessation of training; the differentiation between echocardiographic changes; in highly endurance-trained or combined strength-endurance-trained persons and pathological changes; the importance of heart size and endurance sports performance; and finally the influence of genetic factors.

Echocardiography has become firmly established in cardiological diagnostics in the last few years. With the emergence of technically sophisticated procedures, particularly the 2-dimensional sector scan, echocardiography yields important information, not only about pathological changes, but also about structural and functional adaptations in the healthy heart. Echocardiography is useful to the sports cardiology because it is noninvasive and is repeatable. Measurement is possible with minimal discomfort to the patient which avoids the inaccuracies reported from invasive procedures (Emmerich et al. 1958). In addition, the systematic use of invasive methods or radiography in athletes with healthy hearts would be irresponsible. Furthermore, athletes usually present favourable anatomical conditions for echocardiographic investigations. Using 2-dimensional echocardiography permits better assessment and clearer differentiation between physiological and pathological heart enlargement than a I-beam measurement. In fact, a changed configuration of the ventricle in pathologically enlarged hearts often must be taken into consideration, particularly in functional evaluation (Feigenbaum 1981). Echocardiography is of value for both diagnostic indications and examining healthy persons in sports cardiology. Diagnostic uses include the clarification of conspicuous clinical, radiographic or electrocardiographic findings. In particular, echocardiography can differentiate in many cases between training-induced or pathological changes (such as primary or secondary myocardial diseases) or between dilatation and hypertrophy. Echocardiography allows an evaluation of

functional and structural adaptations of the heart in response to training, especially the changes in the 'athlete's heart'. Moreover, echocardiography allows a routine determination of the heart volume (Dickhuth et al. 1983). The goal of the present paper is to describe echocardiographically determined structural and functional changes in endurance and strength athletes and to compare them with normals. In addition, extreme echocardiographic data in healthy persons are compared with pathological findings to avoid misinterpretations. An enlarged heart in a trained person is a healthy athlete's heart in most, but not all cases. This difficulty in assessment is especially significant because prohibiting an endurancetrained athlete with a healthy heart from participating in sport can result in an acute detraining syndrome. Conversely, training must be reduced in case the heart enlargement is pathological, for instance as a result of myocardial damage.

1. Echocardiographic Findings in Endurance-Trained Athletes 1.1 Total Heart Volume in Different Sports

Changes in heart volume are particularly important if the volume load of the myocardium is chronically increased because of long term aerobic training. Heart size was determined by radiography until a few years ago (e.g. Musshoff & Reindell 1956). The echocardiographic method developed by Dickhuth and coworkers (1983) combines enddiastolic I-dimensional measurements of total left ventricular (LV) diameter on mitral valve and papillar planes with 2-dimensional determination of the long axis on the apical 4-chamber view. The

272

end-diastolic LV volume can be obtained from the modified Simpson rule and correlates highly to the radiographically determined total heart volume. Since a physiological volume load, like that in the athlete's heart, leads to uniform enlargement of all parts of the heart (Reindell et al. 1960), total heart size in persons with healthy hearts can be quite reliable from LV size by means of regression analysis (Dickhuth et al. 1983). The correlation coefficient of 0.90, which we found, indicates a high correspondence between echocardiographically and radiographically determined total heart volumes in persons with healthy hearts, at least over a size range of 600 to 700ml (Urhausen & Kindermann 1987). Knowledge of the adaptative changes of the cardiocirculatory system of endurance-trained athletes prevents misinterpretation of conspicuous myocardial findings. Henschen (1899) reported heart enlargements (assessed exclusively by percussion) in healthy cross-country skiers and introduced the term 'athlete's heart'. He interpreted the athlete's heart as a meaningful physiological adaptation to endurance sports and pointed to dilatation and hypertrophy. Subsequently, his findings were confirmed by radiography and echocardiography. However, for a long time, the cardiac enlargement produced by participating in sports was regarded as a consequence of a myocardical damage or an innate or inflammatory myocardial disease. The reason for the misinterpretation was the improper extrapolation of findings gained from the isolated animal heart in vivo. However, more recent studies have shown that the athlete's heart results from a physiological adaptation to chronic endurance training. Reindell and coworkers (1960) introduced the term 'regulative enlargement' which covers both the physiological hypertrophy of the heart muscle and the so-called regulative dilatation. Left ventricular muscle mass may be up to 75% greater than in untrained persons (Dickhuth et al. 1985). All parts of the heart are enlarged similarly, in contrast to many pathological changes (Linzbach 1948). This uniform enlargement has been confirmed by 2-dimensional echocardiography (Hauser et al. 1985). Other studies (Reindell

Sports Medicine 13 (4) 1992

& Dickhuth 1988), however, point to the possibility of a more pronounced hypertrophy of the right ventricle. As there is a quite constant relationship between heart size and bodyweight in untrained persons of all age-groups, heart volume is usually expressed relative to bodyweight. The average value in untrained healthy males is about II ml/kg bodyweight: the lower and upper limits are 9 and 13 ml/kg, respectively (Kindermann et al. (1974). Hearts larger than 13 ml/kg are considered to be enlarged. Although heart volume in untrained and trained women is about 10% smaller than in men because of differences in lean body mass (standard values for untrained females are about 10 ml/kg bodyweight), there are no gender differences with regard to the percentage enlargement of the heart through training (Kindermann et al. 1974). Children and adolescents are also likely to develop the same cardiocirculatory adaptations to endurance training, including heart enlargement, as adults (Kindermann et al. 1974, 1978;Rost 1982). If older persons perform a regular dynamic training of a certain duration and intensity, they can also develop morphological adaptations up to the end of the seventh decade. This also applies to persons who have not participated in any sport for decades (Child & Barnard 1979; Rost & Hollman 1983). 1.2 Differentiation Between Pathologically and Physiologically Enlarged Hearts The most enlarged athletes' hearts (in absolute terms) are to be found in endurance-trained athletes with high bodyweight. These athletes participate in sports where the bodyweight is not carried by the athlete, e.g. swimming, cycling, rowing. Therefore, their bodyweight is not a limiting factor to performance. The largest heart recorded in the literature, with a volume of 1700ml, was that of a cyclist (Hollman 1965). Rowers also have greatly enlarged hearts (Kindermann et al. 1974).The largest bodyweight-related heart volume was about 20 ml/kg and was found in long distance runners (Kindermann et al. 1974; Reindell et al. 1979). In women, we found the most enlarged athlete's heart

273

Echocardiographic Findings in Athletes

in a marathon runner (19.0 ml/kg bodyweight) while a value of 17 ml/kg bodyweight was reported in a cross-country skier (Medved et al. 1975). Although the so-called critical heart weight is often stated as 500g as an absolute value (Linzbach 1948), it is more correct to assume an upper limit of 7.5 g/kg (Dickhuth et al. 1985) or a size of about 20 ml/kg bodyweight because of the dependence on body dimensions. There is a high correspondence between the echocardiographically determined LV muscle mass and autopsy findings (Staiger et al. 1989). The critical heart weight in our sample was only exceeded by 2 top level ultralong distance runners. The highest body surface area-related value for the LV muscle mass we measured was 165 g/m 2. Elsewhere in the literature a value of 176 g/m 2 was reported in an ultralong distance runner and a canoeist (Pellicia et al. 1991). However, the latter showed an interventricular septum thickness of 16mm with a body surface area of 2.02m 2. The upper limit for non-endurancetrained persons was about 130 g/m? (Urhausen et al. 1990). The exercise performed has to meet certain requirements in order to be an effective stimulus for the development of cardiac dimensional changes, i.e. dynamic exercise oflarger muscle groups reaching a certain duration and intensity (Reindell et al. 1960; Rost & Hollmann 1983). This is usually only possible with training in competitive sports. In physically active persons differentiation between physiological or pathological enlargement of the heart is often problematical, especially if other cardiological findings exist. Essential information can be gained from the athlete's training history. However, physicians who are not educated in sports medicine can find difficulty in assessing the importance of previous sports activities in the development of the athlete's heart. For this reason, we have worked out a rating scale to assess the athlete's sports history (Walter et al. 1985). A highly significant correlation was established between heart size and this score, which evaluates frequency, extent and duration (years) of training in different sports. This shows that an incidence of athlete's heart is much rarer than it is usually assumed and

is unlikely to be found if the volume of exercise per week is less than e.g. 30km running, 100km cycling or IOkm swimming. Exercise without a significant endurance component, like sprint or strength training, will not stimulate heart enlargement even if the training lasts several hours daily (Kindermann et al. 1974; Reindell et al. 1960). Another criterion for the differentiation between physiological and pathological heart enlargement is the relationship between heart size and physical performance. The athlete's heart has a stroke volume corresponding to its dimensions. The heart volume-performance index can be used instead of the relationship between heart volume and stroke volume (Reindell et al. 1960). It indicates the relationship between heart size and the ergometrically determined maximum oxygen pulse. A value over 65 suggests discrepancy between heart size and performance. The echocardiographically determined LV volume should also correlate closely with the maximum oxygen pulse and a quotient of 20 is normally not exceeded in an athlete with a healthy heart (Dickhuth et al. 1983). 1.3 Left Ventricular Measurements and Problematical Findings Left ventricular end-diastolic diameter (LVEDD) increases in endurance-trained athletes (see review in Maron 1986). However, as all parts of the athlete's heart (left and right atrium and ventricle) are enlarged there are only small echocardiographic changes in the LV. However, in M-mode measurements a small increase in l-dimensional measures can correspond to considerable (3-dimensional) changes of the stroke volume. The LVEDD is usually less than 60mm in endurance athletes with normal body size and seldom exceeds 62mm in our findings (maximum 63mm) or elsewhere in the literature (Dickhuth et al. 1987). However, in athletes with large body mass, the ventricular diameter can be greater. We found an LVEDD of 67mm in a rower (weight I05kg and height 202cm) with a corresponding cycle ergometric pertormance of 500W in incremental graded exercise. A pathological cause, such as a dilatative cardiomyo-

274

pathy, has to be excluded in a ventricle dilatation of this magnitude, especially if the ergometric performance is not clearly increased and systolic LV function is decreased (see section 2.5). The highest individual value for LVEDD from 738 male athletes reported by Pellicia et al. (1991) is 66mm. However, the authors disregard the body dimensions in the assessment. A LVEDD of 70mm in a world champion road cyclist was reported by Rost (1982). Findings in cyclists (Nishimura et al. 1980; Shapiro 1984) indicate that training over many years is important in the development of an increased LVEDD. Although the LV wall thickness in endurancetrained athletes seems to be similar to that of controls (Maron 1986; Pelliccia et al. 1991), the wall thickness probably increases because of enlarged internal diameter in order to lower the increased wall tension, according to the rule of Laplace. However, body dimensions, age, gender and the specific sport must also be taken into consideration when assessing LV wall thickness (Pelliccia et al. 1991). In our experience and that of other investigations (Dickhuth et al. 1985; Kindermann & Urhausen 1991; Pelliccia et al. 1991; Urhausen & Kindermann 1989; Urhausen et al. 1989, 1990) a wall thickness of 13mm is rarely exceeded, even when LVEDD is greater than 60mm. Average values of about 14mm, such as those of l-dimensional measurements in swimmers (Shapiro & McKenna 1984) and in basketball players (Roeske et al. 1976) are questionable. Contrary to statements of some authors (Cohen & Segal 1985; Morganroth et al. 1975), wrestling cannot be classified as a predominant isometric exercise. The increased wall thickness in basketball players and wrestlers reported by these authors were not confirmed by other investigators (Shapiro 1984; Wolfe et al. 1985). We and other authors (Pelliccia et al. 1991) all occasionally found LV wall thicknesses of 13 to 16mm in some athletes without pathological findings using noninvasive diagnostic methods. In such cases, hereditary and training-induced changes could not be clearly differentiated. However, such values of LV hypertrophy seem to exist only in certain sports (rowing, triathlon, cycling) and pri-

Sports Medicine 13 (4) 1992

marily in successful athletes or in older athletes who have trained regularly for many years (Pelliccia et al. 1991; Shapiro 1984). An increase in LV wall thickness relative to the internal diameter in triathletes has also been reported (Douglas etal. 1986). However, although the control group was age- and sex-matched, the body dimensions were not taken into account. These findings probably reflect the extremely high volume of training in triathlons which is made possible by the low orthopaedic strain in swimming and cycling in comparison with long distance running. In cyclists, a possible higher isometric strain together with a high volume of training may explain the greater wall thickness (26 to 38%) in comparison with control subjects (Fagard et al. 1983; Snoeckx et al. 1982). The specific haemodynamic conditions of the horizontal position of the body in the water could play an important role in swimming. Physiological adaptations in rowers are influenced by the strength training as well as the extensive endurance training involving a large muscle mass. Moreover, rowers usually possess a clearly increased body mass. The combination of these factors can produce not only a high LVEDD, but also a wall thickness in the upper limit or rather just over. Rost (1982) also found the greatest wall thickness in rowers, whereas cyclists and long distance runners had the greatest body dimension-related values. Pelliccia et al. (1991) found LV wall thicknesses over 13mm only in rowers and canoeists, which the authors attributed to training. The body dimensions were not taken into consideration. The Doppler echocardiographically evaluated diastolic function of those athletes was within normal limits. We found an LV wall thickness of 13.5 to 14.5mm in 6 of 30 male Olympic rowers. A clear concentric hypertrophy with ventricle walls of 14mm and thicker is generally regarded as pathological. The most frequent causes are hypertension, hypertrophic cardiomyopathy and aortic stenosis. Hypertrophic cardiomyopathy is considered to be the most frequent cause of sudden death in young athletes (Maron et al. 1980). Further diagnostic clarification of conspicuously thickened ventricle walls is particularly necessary if the LV

275

Echocardiographic Findings in Athletes

internal diameter is not simultaneously increased, leading to an increased thickness-volume ratio. There are few echocardiographic studies in female athletes. In 209 athletes from various sports (mostly endurance-trained athletes) LV wall thicknesses were at most 11 mm (Pelliccia et al. 1991). A wall thickness of 12mm has occasionally been reported by other authors (Rost 1982)and was also found in our own examinations (female rowers with an LVEDD of over 55mm). On the whole, the body surface-related LV measurements were similar to those in male athletes. With regard to the ratio between LV wall thickness and LVEDD, the values in endurance-trained athletes do not differ significantly from those of untrained individuals (Dickhuth et al. 1985; Sugishita et al. 1983; Urhausen & Kindermann 1989; Urhausen et al. 1990) and are sometimes higher (Fagard et al. 1983). 1.4 Short Term Left Ventricular Adaptations to Endurance Training The disadvantage of the cross-sectional studies mentioned so far is that preselection for greater initial myocardial measures in the exercise groups cannot be excluded. Increases in the LVEDD of 19% in runners (Morganroth et al. 1975) and in cyclists (Nishimura et al. 1980) have been reported in longitudinal studies. The importance of echocardiographic investigations of the LV with regard to the changes in endurance performance seems to be limited because no significant changes in the LV dimensions could be ascertained after improving the maximal aerobic capacity (Peronnet et al. 1980; Ricci et al. 1982; Wolfe et al. 1979). However, untrained subjects were involved in these investigations. At the beginning of the training, functional changes are to be expected before structural myocardial adaptations. However, other studies have found a correlation between V02max and LV values, particularly in trained individuals (see review in Maron 1986). Another review (Schaible & Scheuer 1985) found that significant changes of echocardiographic measures (increase in LVEDD and wall thickness) and of the maximal aerobic ca-

pacity are expected if training for 60 minutes at 70% of the maximal heart rate 4 times weekly for 11 weeks (DeMaria et al. 1978). There may be short term seasonal variances in echocardiographic parameters. For instance, a significant increase of LVEDD and wall thickness or LVEDD alone with no corresponding change in the maximal aerobic capacity was found during intensive training periods in rowers (Wieling et al. 1981). Moreover, wall thickness increased in cyclists during the competitive season (Fagard et al. 1983) and decreased by 3mm after 90 days of deconditioning in comparison with the peak training period (Pelliccia et al. 1991). The most impressive changes were reported by Ehsani et al. (1978) in swimmers. After an onset of training for several months, LVEDD increased by 10% after 1 week of intensive training (2 hours daily during 6 days per week). However the LVEDD did not continue to increase beyond 8 weeks. Over the total period of several months, the LV posterior wall thickness increased by 8%. 1.5 Systolic and Diastolic Left Ventricular Function

The systolic LV function, most often expressed as the fractional shortening, is usually found to be normal in the athlete's heart (Kindermann & Urhausen 1991; Roeske et al. 1976; Rost 1982;Shapiro and McKenna 1984; Simon et al. 1978;Sugishita et al. 1983;Urhausen & Kindermann 1989), but can also be decreased (Sugishita et al. 1983). The early stages of dilatative cardiomyopathy can be difficult to differentiate if the LV internal diameter is increased simultaneously. In the athlete's heart, the fractional shortening normalises during exercise. In contrast, the systolic LV function has increased in only 1 study (Colan et al. 1987). Assessing systolic LV function by the fractional shortening is only useful in persons without any segmental wall motion abnormalities and using an appropriately directed echocardiographic beam (i.e. perpendicular to the myocardial wall). Despite the greater wall thickness in endurancetrained athletes, the diastolic function (early diastolic LV filling, isovolumetric LV relaxation) has

276

been found to be comparable to untrained healthy persons (Douglas et al. 1986; Fagard et al. 1983; Shapiro & McKenna 1984; Urhausen & Kindermann 1989), or even improved (Colan et al. 1985; Matsuda et al. 1983; Staiger et al. 1983).

2. Echocardiographic Findings in Strength-Trained Athletes To accurately assess the possible consequences for the heart of intensive strength-training over many years, several factors must be taken into account. A 2-dimensional control scan should be used to avoid errors in wall thickness measurement, particularly of the interventricular septum, arising from the oblique beam and the inclusion of frequently occurring ventricular trabeculae. Moreover, interpreting obviously discrepant values requires taking into consideration the mode of 1dimensional measurement (e.g. standard position of measurement, Q- or R-wave). Hypertension can also produce changes which mask specific training effects. The echocardiographic findings in hypertensive patients range from altered diastolic left ventricular function and typical concentric hypertrophy to the eccentric hypertrophy with altered systolic function (Fouad et al. 1980; Gibson et al. 1979; Inouye et al. 1984). During strength training sessions (double-leg press), mean intra-arterial blood pressure values have reached 320/250mm Hg in top level bodybuilders, and upper values 480/350mm Hg (McDougall et al. 1985). Resistive training leads to an acute increase of blood pressure without a concomitant rise in cardiac output (Effron 1989; Fleck 1988), giving rise to the possibility that daily strength training might cause chronic hypertension accompanied by corresponding echocardiographic changes. However, several studies have demonstrated normal blood pressure among bodybuilders at rest as well as during cycle ergometer exercise (Colliander & Tesch 1988; Volker et al. 1988; Fleck 1988; Urhausen & Kindermann 1989). Particular attention must be paid to the use of a special larger cuff. Commonly used cuffs often clearly overestimate blood pressure. Finally, the heart rate can also in-

Sports Medicine 13 (4) 1992

fluence the echo cardiographic measurements (DeMaria et al. 1979). Furthermore, it is not only necessary to distinguish between strength and endurance training, but also between different types of strength training. The training of bodybuilders (high repetitions with less resistance) differs from that of weightlifters (low repetitions with heavy resistance). It is necessary to determine whether endurance training is also performed to avoid misinterpreting an enlarged heart in the strength-trained athlete as resulting from strength training. Anabolic steroid use may also influence myocardial parameters in strength athletes (see section 3.4). 2.1 Influence of Body Dimensions Correction for body dimensions is essential in the assessment of echocardiographic measurements, particularly in strength-trained athletes (Brown et al. 1983; Dickhuth et al. 1985; Fleck 1988; Henry et al. 1987; Kindermann & Urhausen 1991; Longhurst et al. 1980; Menapace et al. 1982; Rost 1982; Shapiro 1984; Simon et al. 1979; Urhausen et al. 1990; Urhausen & Kindermann 1989; Wolfe et al. 1986). In our investigations (Urhausen et al. 1989; Urhausen & Kindermann 1989), LV muscle mass enlargement was proportional to the increased lean body mass in all bodybuilders examined. In ove~pportioned not specific trained subjects (Urhausen et al. 1990),the mean body surface of 2.22m2 corresponded exactly to the individual highest value measured by Feigenbaum (1981). The body surface-related measurements of these subjects corresponded to the standard values of the literature. The comparison of strength- and endurance-trained athletes (fig. I) could not confirm the assumption that exists for different mass/ volume ratios between training- and growth-induced changes (Rost 1982). The maximum individual values of the described overproportioned normal persons were 62mm for LVEDD and 13mm for the LV wall thickness. However, correction of myocardial dimensions for lean body mass is possibly more suitable than for body surface area. Some studies have found that the LV measurements were

277

Echocardiographic Findings in Athletes

Absolute LV dimensions (mm)

102

1.4

EDD 54.6

:t 3.7

IVS

PW

10.3 :t 1.3

11.5 _ 1.1

11.2

56.9 :t 4.3

55.6 :t 4.2

11.5

1.1

10.7

1.1

1.4

Body surface area-corrected LV dimensions (mm/m 2 )

5.9 ± 0.7

5.1 :t 0.6

24.6 :t 2.0

29.3 :t 2.6

25.6 :t 2.8

4.6 :t 0.5

5.9 :t 0.8

4.9 :t 0.7

IVS

4.6 :t 0.6

EDD

PW

Untrained

Endurance

trained

Strength

trained

Fig. 1. Mean ± SD echocardiograph ic l-dimensional absolute and body surface area-corrected left ventricular dimensions in health y persons with a body surface area > 2.lm 2 (mean ~ 2.22m 2), in endurance-trained and stero id-free strength-trained athletes (modified from Urhausen et al. 1990). For abbrev iations see table I.

Salke et al. 1985; Snoeckx et al 1982; Sugishita et al. 1983). However, the studies discussed below show that this opinion is no longer tenable. LVEDD is not decreased in resistance-trained athletes, in contrast to findings in pathological pressure load and various forms of cardiomyopathy (Colan et al. 1987; Dickhuth et al. 1987; Longhurst et al. 1980; Menapace et al. 1982; Pearson et al. 1986; Rost 1982; Snoeckx et al. 1982; Urhausen & Kindermann 1989; Urhausen et al. 1990; Van Den Broeke & Fagard 1988). In cases with different body proportions, the LVEDD found in a few resistance-trained athletes can be even higher than that in endurance-trained athletes (Shapiro 1984). Increased absolute values for the LV wall thickness were reported by Colan et al. (1987), Menapace et al. (1982), Morganroth et al. (1975) and Saike et al. (1985) [table I]. The body surface areacorrected LV muscle mass was clearly increased only in Colan et al. (1987). In our own findings, we did not find any strength athlete (both with and without intake of anabolic steroids) with a LV muscle mass of over 3.5 g/kg, which is the critical heart weight (Dickhuth et al. 1985; Staiger et al. 1989). When evaluating these values, several points should be noted. With the exception of Colan et

•

Anabol ic

steroid users

Nonusers

greater in strength athletes than those in controls when corrected for body surface area but not when corrected for lean body mass (Brown et al. 1983; Longhurst et al. 1980). 2.2 Left Ventricular Measurements and Problematical Findings Several researchers have reported that athletes engaging in mainly isometric exercise developed increased LV wall thickness similar to the concentric hypertrophy observed in chronic pressure overload (Cohen & Segal 1985; Dickhuth et al. 1979; Longhust et al. 1980; Morganroth et al. 1975;

fo.

SO.70 60

,....- .

~

~

0.50

..

--,

0.40

~ 0.50

.§ 0.40

0.30

~ 0.30

0.20

::i

0.10

'5 0.20

0.10 EDD

iVS

FIg. 2. One-dimensional left ventricular (LV) diameter and wall thickness/diameter ratio in using anabolic steroids compared to nonusers ations see table I) [means ± SO; statistics: • •• ~ p < 0.01) [Urhausen et al. 1989].

+ LVPW I

EDD

end-diastolic bodybuilders (for abbrevi~ p < 0.05;

278

Sports Medicine 13 (4) 1992

Table I. Review of echocardiographic studies of resistance-trained athletes. Only control groups including comparable body dimensions are considered. Left ventricular (LV) parameters: EDD = end-diastolic diameter; IVS = interventricular septum; PW = posterior

wall; MM

= muscle mass. Values are reported

Reference

Morganroth et al. (1975) Dickhuth et al. (1979) Longhurst et al. (1990)

Menapace et al. (1982) Rost (1982) Snoeckx et al. (1982) Brown et al. (1983) Shapiro (1984)

Salke et al. 1985 Pearson et al. (1986) Colan et al. (1987) Roy et al. (1988) Van den Brooke and Fagard (1988) Urhausen et al. (1989) Urhausen et al. (1990)

as means

Subjects

4 9 15 17 7 10 13 8 14 17 18 9 34

15 15 16 11 46 10 10 14 7 12

shotputters weightlifters athletic putters, throwers competitive weightlifters recreational weightlifters heavy controls weightlifters (top level) weightlifters weightlifters controls weightlifters heavy controls athletic throwers and weightlifters

Body surface (m2)

2.52 2.3c 2.11 2.03 2.11 2.05 2.30 1.92c 1.82 1.88 2.00 12

EDD (mm)

(mm)

IVS

PW (mm)

MM (g/m 2)a

46-51 50.6 51.5 54 52 54 51.5 55.9 51-51.5 d 50.4 55.4 55.3 54

13.5 12.6 12.6 9.3 9.7 8.3 13.9 12.1 9-9.5d 8.5 8.8 8.6 12.5

13.8 10.3 10.9 9.5 8.5 8.2 9.7 10.4 9-9.5d 8.2 9.4 8.9 10.5

138b

53.1 52.4 56 54 55 52.8 50.1 54.7 57.4 56

13.7 12.4 10

9.4 9.4 9 13.2 9.6 10.5 10.5 12.5 10.3 10.7

91 86 72

134 116 159 9

subjects>

2.2 2.13 steroid-using bodybuilders 2.05 steroid-free bodybuilders 2.1 weightlifters 2.28 powerlifters 2.02 bodybuilders athletic throwers 2.08 2.08 heavy controls steroid-using bodybuilders 2.12 steroid-free 2.09 steroid-free resistance-trained 2.19

10.1 10.7 12.6 11.6 11.2

114 165 131 b

111' 102 103

athletes Pelliccia et al. (1991)

a b c d e f

32 heavy controls 9 (19) weight-lifters 7 heavy controls

2.22 2.26 1.96

55 55.5 53.2

10.3

10.3 10.0 10.4

93 91 100

Calculated by Devereux and Reichek (1977). Calculated by Troy et al. (1972). Calculated by means of height and weight. Estimated on figures. Calculated by cube volume formula. Calculated by Dickhuth et al. (1983).

al. (1987) M-mode measurements were used without 2-dimensional control. A possible intake of anabolic steroids was just taken into consideration by Salke et al. (1985). In the findings of Morganroth et al. (1975), the 4 athletes examined had extreme body dimensions, so that the LVEDD decreased relative to the body surface area. Moreover, some

authors found a disproportionate thickening of the septum in comparison to the LV free wall in many (Longhust et al. 1980; Salke et al. 1985) or even all subjects (Menapace et al. 1982) without there being any indication of asymmetric septum hypertrophy (Gilbert et al. 1980; Henry et al. 1973). In other studies, this ratio was within the normal range

279

Echocardiographic Findings in Athletes

(Dickhuth et al. 1987; Morganroth et al. 1975; Pearson et al. 1986; Rost 1982; Rost & Hollmann 1983; Urhausen et al. 1989, 1990; Van Den Broeke & Fagard 1988). In our experience and according to Rost (1982), higher values are often attributable to a thinner LV posterior wall than to a thickening of the septum. Shapiro (1984) found a septum/Lv posterior wall ratio over 1.3 in 21% of the strength athletes and concluded that the septal thickening may be a normal manifestation of secondary LV hypertrophy of whatever cause. This statement, however, cannot be confirmed by studies performed with overproportioned controls (see table I). In addition, other authors suggest that wall thickness may depend on competitive level (Shapiro 1984). However, we found an interventricular septum thickness of only 12mm even in an Olympic medalist in weightlifting with a bodyweight of almost 150kg. These findings suggest that regardless of whether heart enlargement is due to an athletic heart or to greater body dimensions, in healthy persons a regular mass/volume ratio is maintained. The fact that in resistance- and endurance-trained athletes as well as in overdimensioned untrained persons the thicker LV walls are accompanied by greater internal diameters appears to be essential in differentiating between physiological and pathological hypertrophy (Dickhuth et al. 1985; Keul et al 1981; Staiger et al. 1989). On the whole, the thickest walls of the left ventricle are to be found in hearts with the greatest internal diameters under physiological conditions. 2.3 Systolic and Diastolic Left Ventricular Function It is a common finding that the systolic contractility of predominantly isometrically trained athletes lies within the normal range. In only 1 study (Colan et al. 1987) was the fractional shortening augmented, and this was attributed to altered loading conditions caused by ventricular hypertrophy and dilatation. The diastolic LV function in resistance-trained athletes was also found to be normal (Pearson et al. 1986; Urhausen & Kinder-

mann 1989; Urhausen et al. 1990; Van Den Broeke & Fagard 1988) or even improved (Colan et al. 1985). The right ventricle could not be evaluated adequately in echocardiographic examinations previously because of methodological problems. In a recent study using magnetic resonance imaging, Olympic weightlifters showed left, but no right, ventricular wall hypertrophy (Fleck et al. 1989). 2.4 Influence of Anabolic Steroids on the Myocardium It is assumed today that the intake of anabolic steroids with a corresponding high intensity of training results in muscle growth (Alen et al. 1984; American College of Sports Medicine 1984), although there has long been controversy concerning the strength-increasing effect of anabolic steroids. The intake of anabolic steroids during training is, therefore, relatively widespread in those sports in which a large muscle mass is an advantage. Hypertrophy of the heart muscle comparable to that in skeletal muscle has been demonstrated in earlier studies (Blasius et al. 1957). More recent investigations report pathological changes in myo-

cardial cells induced by anabolic drugs. In addition to biochemical alterations, particularly a reduced LDH fraction (Weicker et al. 1982), ultrastructural investigations showed aberrant and chaotically spaced myofibrils which were partially altered or destroyed, as well as intracellular oedema and mitochondrial swelling (Appell et al. 1983; Behrendt & Boffin 1977). However, the possible influence of anabolic steroids in predominantly isometrically trained athletes has only been taken into account by echocardiography in a few studies (Pearson et al. 1986; Salke et al. 1985; Ullrich et al. 1990; Urhausen et al. 1989; Zuliani et al. 1989). In contrast to the other studies, Salke et al. (1985) found no significant differences between anabolic steroid users and nonusers. In this study, however, it is remarkable that both groups of bodybuilders showed a clearly increased septum/Lv posterior wall ratio (mean 1.47 and 1.36). Here, it has to be pointed out that measurements were l-dimen-

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sional without 2-dimensional control, and there is the danger of erroneous dimensions indicating an overly thickened interventricular septum. Whereas there was a simultaneous increase in LV wall thickness and inner volume in the nonusers or anabolic steroids, disproportionate mycardial hypertrophy with a smaller LV internal diameter relative to bodyweight, and thus a higher mass/volume ratio, was found in bodybuilders regularly taking anabolic steroids (Urhausen et al. 1989) [fig. 2]. This was confirmed by other studies (Pearson et al. 1986; Ullrich et al. 1990). The ratio between LV myocardial thickness and internal diameter in our anabolic steroid users was very similar to values obtained for weightlifters in a previous study (Menapace et al. 1982) in which possible anabolic steroid consumption was not taken into consideration. In this study, the control group showed similar ratio to our nonusers. In none of the nonusers was a diastolic septum or posterior wall thickness exceeding 13mm measured, whereas this was the case in II of the 14 anabolic steroid users (Urhausen et al. 1989). With regard to a body surface area-corrected increase in LV muscle mass in strength athletes (Longhurst et al. 1980; Pearson et al. 1986; Ullrich et al. 1990),it can be speculated that an intake of anabolic steroids makes possible an increase in lean body mass which cannot be reached under physiological conditions. The LV muscle mass could increase in parallel. However, in our study (Urhausen et al. 1989), no significant correlation between the moderate concentric hypertrophy and the lean body mass was found in anabolic steroid users. An interesting parallel exists to previous findings of concentric hypertrophy in patients with acromegaly due to increased growth hormone secretion (Bodem et al. 1978). The moderate concentric wall thickening in anabolic steroid users, however, did not attain the values of concentric hypertrophy observed in hypertension or hypertrophic cardiomyopathy (Dickhuth et al. 1987; Henry et al. 1973; Menapace et al. 1982; Urhausen et al. 1989). In contrast to a hypertrophic cardiomyopathy, there was normal systolic wall movement and fractional shortening without pathological ECG findings.

Sports Medicine 13 (4) 1992

Some investigators found impaired LV diastolic function in anabolic steroid users (Pearson et al. 1986; Urhausen et al. 1989), although this is not a universal finding (Ullrich et al. 1990). The dosage and the duration of intake of anabolic steroids are possibly of importance just as in LV hypertrophy; Pearson et al. (1986) found a significant negative correlation between the index of steroid intake and the rapid LV filling. In the study of Roy et al. (1988), half of the examined bodybuilders admitted to have taken steroids; even so, the index of hypertrophy was in normal range. Zuliani et al. (1989) did not find significant changes of the echocardiographically measured parameters after 8 weeks of anabolic steroid use and strength training. If the diastolic function is impaired, it seems to be independent of the wall thickness or LV muscle mass itself (Colan et al. 1985; Pearson et al. 1986; Shapiro & McKenna 1984; Urhausen et al. 1989). In our study (Urhausen et al. 1989), the most pronounced prolongation in isovolumetric relaxation was found in those athletes showing the highest hypertrophy index, as indicated by the ratio between wall thickness and internal diameter. The shortest isovolumetric relaxation times were obtained for those bodybuilders with the lowest hypertrophy index. The isovolumetric relaxation time index measured echocardiographically as a parameter of the diastolic function correlates to a highly significant degree with the true isovolumetric relaxation time (Hanrath et al. 1980). A higher index could already be noted in the early stages of a hypertension when no hypertrophy can yet be measured. A diminished calcium reuptake in the sarcoplasmatic reticulum might be responsible for this delayed relaxation time (Lecarpentier et al. 1984). The early diastolic filling velocity, on the other hand, appears not to decrease until a relatively advanced stage of hypertension, accompanied by abnormal wall thickening with ischaemic or fibrotic processes possibly being attributable (Shapiro & McKenna et al. 1984). Despite measurable wall hypertrophy, the early diastolic filling velocity in the anabolic steroid users was not delayed (Urhausen et al. 1989). Corresponding studies in the literature report that echocardiographic measurements of the early dia-

Echocardiographic Findings in Athletes

stolic filling velocity allowed for a delineation to be made between forms of physiological and pathological primary or secondary hypertrophy (Colan et al. 1985). In conclusion, it is assumed that the intake or anabolic steroids, combined with intensive strength training can lead to a moderate concentric increase in the LV wall thickness and impaired diastolic function.

3. Future Research The morphological adaptations of the right ventricle induced by endurance and strength training await further research. Echocardiography offers only limited possibilities for the assessment of the right ventricle. New findings can be expected from magnetic resonance imaging. The regression of the heart enlargement with increased age and decreased physical activity also remains to be investigated. Do the morphological and functional adaptations in the myocardium regress completely (VollmerLarsen et al. 1989) or only partially (Dickhuth et al. 1989) over several years? In an echocardiographic study in former endurance athletes (mean age 66 years) with a radiographically slightly enlarged heart size, LVEDD was similar to a control group of the same age, but the left atrium was significantly increased, which was probably related to the previous training (Hoglund 1986). However, 5 out of the 13 subjects also showed an increased incidence of supraventricular arrhythmias. In addition, genetic influences like moderately enlarged hearts or predisposition for their development must be taken into consideration if evaluating enlarged hearts in former endurance athletes. Moreover, the speed with which heart size decreases after cessation of training is still unclear. A regression of the heart size by 10 to 15% within 3 weeks can be expected in complete immobilisation (Saltin et al. 1968). According to our own experience and the opinion of other authors (Dickhuth et al. 1989), a relatively small amount of regular endurance exercise could be enough to preserve important cardiovascular adaptations including an enlarged heart. However, genetic factors may also influence these

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changes. Finally, the aptitude for endurance sports may derive from an innate athlete's heart. Rost et al. (1989) did not find any clear echocardiographic evidence of such a congenital athlete's heart out of 131 children.

4. Conclusions The development of the so-called athlete's heart in highly endurance-trained athletes depends on the intensity and duration of training. The uniformly enlarged and healthy heart is associated with enhanced performance and is characterised by an increase of the internal volumes and the wall thickness so that the standard body dimension-corrected values are exceeded. In isometrically trained athletes, the echocardiographic measures increase in parallel to the body dimensions; the active body mass is of special importance in these subjects. The ratio between LV myocardial mass and internal volume is not significantly different in strength athletes in comparison to endurance-trained ones. However, anabolic steroid use can lead to a moderate concentric hypertrophy and impaired diastolic function. Therefore, the echocardiographic finding of a myocardial wall thickening in strength athletes may be attributed to additional influences, such as hypertension, aortic stenosis, cardiomyopathy or an intake of anabolic steroids. Echocardiographic measures should always be corrected for body dimensions, especially in persons with larger body mass. However, whereas the absolute echocardiographic values for the LVEDD can be often exceeded in a physiological heart enlargement, the wall thickness does not generally exceed the upper range and is seldom over l3mm.

Acknowledgement Supported by the Bundesinstitut fur Sportwissenschaft, Cologne (no. 0407/01/06/87 and 0407/01/06/88).

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Correspondence and reprints: Dr A. Urhausen, Institute of Sports and Performance Medicine, University of Saarland, D-66oo Saarbriicken, Federal Republic of Germany.