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Do athletes have “the athlete heart?”
Do Athletes Have “The Athlete Heart?” HELENE M. PERRAULT, PH.D. RENE A. TURCOTTE, PH.D. Department of Physical Education McGill University Montreal. Canada
In 1897 Henschen’ used cutaneous percussion to examine the hearts of cross-country skiers and reported that those with larger hearts also had better placements in the race. Nearly 100 years later and after several hundred publications, the significance of this observation is still debated. The term, “athlete heart,” was introduced to describe the cardiovascular effects of exercise in competitive athletes. Two decades ago accurate direct in vivo measurements of cardiac structures became feasible for the first time with the introduction of echocardiography. Between 1975 and 1992, more than 80 studies compared left ventricular (LV) morphology in more than 1000 nonathletes and athletes with endurance or strength fitness (Table l), and 20 other studies examined the changes in LV structure of healthy sedentary individuals following predominantly endurance-type training programs (Table 2). The common interpretation of these observations is that regular physical activity induces cardiac hypertrophy . However, a large number of confounding factors have not been considered in the interpretation of these data. This paper will critically review the scientific literature concerning cardiac morphological adaptations to training in humans that suggests that athletes, in fact, may have rather “normal” cardiac dimensions. Address correspondence to Dr. Helene M. Perrault, Service de Cardiologie et de Medecine Pulmonaire, HBpital Ste-Justine, 3175 Chemin Cote Ste-Catherine, Montreal, Quebec, Canada, H3T lC5.
MORPHOLOGY OF THE ATHLETE HEART: REVIEW OF ECHOCARDIOCRAPHIC DATA Two different methodological approaches have been used in the echocardiographic examination of cardiac morphology. Studies with cross-sectional design have compared LV structures of athletes involved in different sport disciplines to those of sedentary “nonathletes,” whereas studies with longitudinal design have examined changes in these structures before and after several weeks or months of regular physical training. In most studies LV enddiastolic measurements have included internal diameter (LVEDD) and posterior wall thickness (LVPW), with interventricular septal wall thickness reported in only some cases. The results of a metaanalysis of findings from cross-sectional comparisons of sedentary controls to endurance- or strengthtrained athletes appear in Figures 1 and 2, respectively (see Table 1 for references). The average LV dimensions calculated from the reported group means in each study is shown as well as the weighted mean, calculated from the overall average of group means, weighted for the number of individual observations in each group. As seen in Figure 1, no difference can be observed between weighted means and group means of endurance athletes or their sedentary controls, reflecting the homogeneity in echocardiographic measurements of LV structures both in these athletes and in controls. Statistical analysis of the results indicates significant differences in LV morphological characProg Pediatr Cardiol 1993; 2(2):40-50 Copyright 0 1993 by Andover Medical
The Athlete Heart
TABLE
1. Cross-Sectional Echocardiographic
41
Studies of Athletes
Reference
Comparisons
N/Category
Morganroth et al. (1975) Rost et al. (1975) Lemon et ai. (1976) Nutter et al. (1976) Houdas et al. (1976) Roeske et a1. (1976) Falsetti et al. (1977) Fannapazir et al. (1982) Gilbert et al. (1977) Howald et al. (1977) Underwood et al. (1977) Laurenceau et al. (1978) Parker et al. (1978) Quiret et al. (1978) Zeldis et al. (1978) Grayevskaya et al. (1979) Ikaheimo et al. (1979) Monnet et al. (1979) Zoneraich et al. (1979) Adda et al. (1981) Blair et al. (1980) Cohen et al. (1980) Drescher et al. (‘1980) Lesbre et al. (1980) Longhurst et al. (1980) Nishimura et al. (1980) Kanakis et al. (1980) Bose et al. (1980) Bekaert et al. (1981) Fisher et al. (1981) Keul et al, (1981) Mumford et al. (1981) Paulsen et al. (1981) Rubal et al. (1981) Heath et al. (1981) Menapace et al. (1982) Snoeckx et al. (1982) Wieling et al. (1982) Fagard et al. (1983) Sugishita et al. (1983) Spirit0 et al. (1983) Child et al. (1984) Moore et al. (1984) Shapiro (1984) Shaviro and Mckenna (1984) . Cohen et al. (1985) Golan et al. (1985) Hauser et al. (1985) SJongers et al. (1985) Sparato et al. (1985) Wolfe et al. (1985) Csanady et al. (1986) Fargard et al. (1987) Van Den Brocke et al, (1988) Dickhuth et al. (1989) Fisher et al. (1989) Sepulveda et al. (1989) Percy et al. (1990)
C/E/R
16/15/14 10
; C/E R C/E E C/E C/E C/E C/E C/E C/E E E C/E C/E C/E C/E
26/20 1000 18 26120 818 10/20 12/11 15 25 31/152 13/12 32/28 20/12
C/E C/E C/E C/E/R C/E/R C/E
20/20 15130 75/21 -/20/10 10/12/17 35160
C/R
15/29 11/14
C/E R C/E/R C/E C/E C/E C/E C/R C/E E C/E C/E/R C/R C/E/R C/E C/E/R C/E C/E/R C/E/R C/E C/E C/E/R C/E E C/E C/R C/E C/E C/E
19/19 1018 10/9 18/32 10113 17131 23 12/12 14131/17 12/9/13 14114 40/104134 20/10 10/10/10 22111111 lo/11 501194/69 13/11 29 16/16 lO/lO 7/7 20122 14110
This table lists echocardiographic studies that have been considered in the computation of average LV dimensions found in sedentary controls (C), endurance athletes (E), and resistance- or power-trained athletes (R). When available, the number of controls, endurance, or resistance athletes examined is also shown.
Progress in Pediatric Cardiology
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TABLE 2. Longitudinal Echocardiographic
Studies of Athletes
Reference
Type
Duration (weeks)
N/Category
Frick et al. (1970) Houdas et al. (1976) DeMaria et al. (1978) Ehsani et al. (1978) Wolfe et al. (1979) Michielli et al. (1979) Righetti et al. (1980) Teronnet et al. (1980) Perrault et al. (1982) Ricci et al. (1982) Wazana et al. (1980) Adda et al. (1981) Thompson et al. (1981) Wieling et al. (1981) Adams et al. (1985) Hickson et al. (1985) Wolfe et al. (1985) Cox et al. (1986) Younis et al. (1987) Rubal et al. (1987) Martin III et al. (1986)
E E E E E E E E E E/R E E E E E E E E E E D
8 28 11 9 24 14 10 20 20 8/20 52 11 11 28 14 10 30 7 24 10 3/8/12
20 15 24 8 15 14 18 11 14 8/20 26 11 10 23 50 12 12 11 19 10 6
This table presentsechocardiographicstudies that have been considered in the computation of average LV dimensionsbefore and after endurance(E) or resistance(R) training or after deconditioning (D). The duration of training is provided in the middle column.
ECHOCARDIOGRAPHIC “. 1375 endurance athletes SO
STUDIES
n-340
(19751991)
‘resistance”
athletes
and 255
controls
and 748 controls
1
LVEDD (mm)
Y
LVEODCmm)
LVPWCmm)
Heart
I
*,I?,. mean
Bsa Alill. weighted mean
0
cont. mean
lllwl
LVPWd (mm)
rate(bpm)
Cont. wsighted mean
Figure 1. Summary of the findings of cross-sectional designed echocardiographic studies conducted between 1975 and 1991, comparing LV dimensions of endurance athletes with nonathletic controls. Calculated means + standard deviations from all groups of athletes and controls are shown in filled and dotted bars. Weighted means, calculated according to the number of observations per group, are shown in diagonal and vertical hatched bars. *Statistical significance (F’ < .05) between athletes and controls.
1
LVEDDfSSA
I
Afhl. mean
@a
0
cant. mean
lllwn cont. Weighted mean
LVPWdIBSA
AthI. weighted mean
Figure 2. Summary of the findings of cross-sectional designed echocardiographic studies conducted between 7975 and 1991, comparing LV dimensions in resistance athletes with nonathletic controls. (A) Shows the calculated means f standard deviations for all groups of athletes and nonathletes in filled and dotted bars, as well as the computed weighted means in diagonal and vertical hatching. (B) Illustrates the calculated means _t standard deviations of LV dimensions, corrected for BSA in resistance athletes and nonathletes. Ytatistical significance (P < .05) between athletes and nonathletes.
The Athlete Heart
teristics between groups. The average dimensions calculated for LVEDD and LVPW in over 1200 endurance athletes are 53.5 f 3.4 mm and lo.2 f 1.5 mm, respectively, whereas those of some 800 age-matched controls are 48.2 f 2.2 mm and 8.66 f 1.1 mm. Calculated average resting heart rates were 55 + 5 bpm and 66 k 6 bpm, respectively, in athletes and controls. As first shown by Morganroth et a1.2 cardiac dimensions measured in resistance- or strength-trained athletes are different from those observed in endurance athletes, with mean LVEDD and LVPW calculations in a total of 340 athletes in 25 studies of 52.2 f 2.2 mm and 11.2 + 1.5 mm, respectively (Figure 2). The classification of some sports in terms of resistance or strength attributes is not as easily established as for pure endurance events. Consequently, classification designations are based frequently on an exclusion criteria of an endurance sport and include athletes from a number of various disciplines such as judo, shotput, discus throw, weight lifting, body building, and sprint running. The wide variation in the selection of subjects from one study to another may be seen in the differences observed between weighted and group means. Application of statistical analyses to the overall group means of endurance athletes, strength athletes, and controls indicate significant differences (p < .05) between groups, although the validity of the analysis may be questioned because of the inhomogeneity of variance between groups. A summary of the echocardiographic data from longitudinal investigations of healthy sedentary individuals is presented in Figure 3 (see Table 2). In all cases, values are comparable to those found in sedentary controls in the previous cross-sectional studies, with average values calculated in 257 subjects of 49.1 + 3.0 mm and 9.3 f 1.2 mm for LVEDD and LVPW. After 4 to 52 weeks of endurance training (average 18 weeks), the calculated average dimensions were 51.6 f 2.9 mm and 9.6 f 1.1 mm, showing statistically significant increases. No relationship, however, could be calculated between the training duration and the magnitude of change in LV dimensions. These data are not new. They merely provide an up-date of numerous earlier reviews.3-5 In the next section, however, several factors will be discussed that may have biased the interpretation of these studies. Three methodological problems and sev-
43
M
LONGITUDINAL
STUDIES
(29751990)
Figure 3. Comparisons of the LV free wall and cavity dimensions of sedentary individuals before training with measurements in sedentary controls from crosssectional designed studies (top), after training (middle), endurance athletes from cross-sectional studies (second from bottom), and resistance athletes from cross-sectional studies (bottom). The number of studies from which the mean values are calculated is shown by n.
era1 confounding factors of training need to be addressed.
METHODOLOGICAL
CONSIDERATIONS
Accuracy of the Measuring Tool One limitation of ultrasound measurements is axial resolution, the smallest distance between two structures that actually can be distinguished. Ultrasonic transducers generally used in adult echocardiographic studies have frequencies between 2.25 MHz and 3.0 MHz with an axial resolution of approximately 2.2 mm.6,7 However, in echocardiographic measurements of LVPW, differences between endurance athletes and controls (Table 1 references) range between 1.4 mm and 5.0 mm (average 1.6 mm). Similarly, after an endurance training program, pre- to posttraining differences in LVPW range from -0.6 mm to 1.0 mm (average change 0.34 f 0.46 mm) (Table 2 references). These differences remain below the limit of axial resolution of the echocardiographic technique. An aver-
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age difference of 5.5 mm (range 2.2 mm to 10.2 mm) is measured between the average LVEDD of athletes and controls, whereas pre- to posttraining differences range from 0.30 mm to 4.60 mm (average change 2.1 mm), at the limit of the resolution of the technique. It is important to appreciate that although statistical analyses provide a means to quantify the difference between group means, they do not indicate the theoretical or physiologic significance of the findings. Thus, for cardiac dimensions measured by echocardiography, statistically significant differences are meaningless unless they exceed the limit of axial resolution. Left Ventricular
Mass Index
The capacity for myocardial hypertrophy in response to systolic or diastolic pressure and volume overload has been well documented in animal models.8-11 In animals with aortic constriction, a significant increase (17%) in LV mass has been reported after 72 hours of aortic obstruction.8 Continuous LV volume overload was associated with an increase in mass of 14% after 1 week of application and an increase of 30% after 8 weeks.‘O In humans, ventricular hypertrophy can also be observed in response to conditions of continuous pressure or volume overload.“-l3 However, consider the extent of overload produced by physical training programs in humans. In most of the studies reviewed, the training programs consisted of moderate volume (endurance training) or pressure (strength training) overload for 1 hour and, exceptionally, 2 hours a day, 3 to 6 days a week for a total of 3 to 12 hours of exercise a week (Table 2). Yet changes in LV mass of approximately 30 % have been reported after only 2 weeks of training, corresponding to 6 or 8 hours of swimming (Ehsani et al. Table 2). Although it is tempting to conclude that this reflects a true myocardial hypertrophic response to training, other interpretations need to be considered. Left Ventricular
Volume
Left ventricular mass is calculated by subtracting values of internal LV volume from total LV volume, multiplied by specific gravity of cardiac muscle.6 Calculation of LV volume, in turn, relies on the assumption that the LV geometry is ellipsoidal, spherical, or cubic. In any of these models, computation of LV volume is based on the application of
a cubic function to the LV radius or the LVEDD. Depending on the equation used, differences from 15 % to 20% can be found in calculated LV volume, which limits the usefulness of such estimations of absolute LV volume. In addition, because of the cubed effect inherent in the computation of LV volume, small and nonsignificant differences in LV dimensions and measurement errors can become inflated, resulting in statistically significant differences. For example, consider the change in LV mass resulting from a l-mm increase in LVPW with no change in LVEDD. Although the basic change in LVPW with training is below the resolution of the measurement technique, a significant 15 % increase in “calculated” LV mass can be reported. This is not dissimilar to changes reported following endurance training, although an increase in LVEDD is usually also reported (Table 2). The question remains, however, as to whether this reflects a “true” increase in muscle mass.
CONFOUNDING FACTORS ASSOCIATED WITH LONGITUDINAL STUDIES By convention, the echocardiographic measurement of LVEDD is made in phase with the R wave of a simultaneously recorded electrocardiographic (ECG) tracing. This implies that changes in the R-R interval will affect the echocardiographic measurement of LVEDD. Similarly, changes in total blood volume caused by pharmacologic, pathologic, or physiologic conditions will affect it .i4-18Two factors associated with physical training, heart rate, and blood volume can affect LV diastolic filling and can change LVEDD without changing true LV mass. These are confounding factors associated with training, which should be taken into account in the interpretation of the echocardiographic data. Influence
of Sinus Node
Variability
The first confounding factor to consider is resting heart rate. Resting bradycardia is a well-known and widely accepted index of endurance training. In the present review of echocardiographic longitudinal studies, a difference of 11bpm is found between the average resting heart rates reported in endurance athletes and control subjects (Figure 3). Similarly, the echocardiographic examination of subjects following an endurance training program is associated with a significantly lower resting heart rate. The
The Athlete Heart
average change in heart rate calculated from the endurance training studies, reported in Figure 3, is 7 bpm. However, differences in resting heart rates have not been considered in the interpretation of echocardiographic measurements made after endurance training or in comparisons of endurancetrained athletes with sedentary controls. The effects of heart rate variations on LV internal diameter have been well documented. Using atria1 pacing, DeMaria et a1.14established an inverse linear relationship between LVEDD and heart rate, demonstrating that a IO-beat increment in resting heart rate is accompanied by a 2.7% decrease in LVEDD. Application of the prediction equation for LVEDD to the difference in resting heart rates in athletes and nonathletes (Figure 1) results in a difference of 1.4 mm in LVEDD. Similarly, according to the average calculated bradycardic response after endurance training studies, a l-mm increase in LVEDD could be predicted. Although this remains below the average change of 2.1 mm in LVEDD reported following training, these observations suggest that training bradycardia can account for a portion of the differences reported between endurance athletes and nonathletes following training. A regression analysis of the LVEDD and heart rates in 55 of the cross-sectional studies of athletes and controls indicates a significant correlation (r = 0.63) between these two variables. Efects of Endurance Training on Total Blood Volume Changes in the echocardiographic measurement of LVEDD have also been associated with changes in plasma volume or total blood volume, a second confounding factor. On retuning from an &day exposure to microgravity, space crew members showed a significant plasma volume contraction associated with a 23% decrease in echocardiographic determinations of LVEDD volume index.15 Conversely, significant increases in LVEDD have been reported following plasma volume expansion associated with pregnancy16st7 or after a change from upright to supine posture.18*19Chronic hypervolemia also occurs as a result of endurance training because of an increase in the total circulating plasma levels of electrolytes and proteins.20 Results from cross-sectional comparisons clearly indicate that endurance-trained athletes have 20% to 25% larger blood volumes than untrained subjects. Lon-
45
gitudinal studies of adaptations of blood volume to endurance training show that an increase can be measured after a single bout of exercise, and that a plateau is reached after only 1 week of training, with blood volume expansions ranging from 5% to 10% .21Similar increases in plasma volume with postural changes have been found to produce increases in LVEDD of up to 5 mm.22J3 Moreover, recent studies of highly trained athletes showed a S-mm decrease in the upright measurement of LVEDD after only 3 weeks of deconditioning, associated with a decrease in cardiac preload volume.24 Thus, the training effects on echocardiographic measurements of LVEDD are best explained by ventricular dilation due to training bradycardia and hypervolemia rather than by true eccentric cardiac hypertrophy. The argument against this view assumes that only stretching of the existing LV chamber without a concurrent increase in ventricular muscle mass results in a thinning of the wall, similar to that of a stretched balloon. However, from the equation for LV mass, it can be calculated that the difference in wall thickness produced by an increase in LVEDD of 2.2 mm (average change reported) without a change in LV mass would amount to a 0.5-mm decrease in LVPW, which essentially is too small to be detected by echocardiography.
CONFOUNDING FACTORS ASSOCIATED WITH CROSS-SECTIONAL COMPARISONS Cross-sectional LV echocardiographic measurements have also been used to indicate a direct effect of physical training on cardiac morphology. Although directional differences between trained and untrained subjects may be provided by such comparisons, they do not distinguish between the direct results of training and the effects of physical and physiologic factors. For example, differences in cardiac loading conditions from training-induced bradycardia or chronic hypervolemia have not been considered in the echocardiographic evaluations of endurance athletes, and cross-sectional design comparisons of measurements in athletes and nonathletes have often failed to consider the inffuence of anthropometric characteristics on cardiac dimensions.
46
Progress in Pediatric Cardiology
Body Dimensions The influence of body size on heart size is well documented. A number of early echocardiographic investigations in both children and adults6~25*26 and more recent results from the Framingham studyz7 have established significant correlations of LVEDD and LVPW with body surface area (BSA), body mass, and lean body mass. The influence of body size, however, was not considered in the interpretation of comparisons of cross-sectional echocardiographic cardiac dimensions in athletes and nonathletes. In athletes involved primarily in resistance-type and endurance-type training, initial comparisons led to the popular theory of sport-specific patterns of cardiac morphology. Results showed that resistance athletes had significantly larger LVPW (Figure 2) than that seen in endurance athletes, presumably because of the high pressure overload associated with their sport discipline. However, more recent study has shown (Fisher et al. Table l), that the difference in LVPW is greatly attenuated when values are corrected for BSA. In the compilation of results presented here, correction of LV dimensions reported in cross-sectional echocardiographic studies where BSA was either provided or could be calculated (Figure 2), resulted in corrected LVPW/ BSA values of 4.9 mm/m* in controls (26 studies), 5.6 mm/m2 in endurance athletes (35 studies), and 5.5 mm/m2 in resistance or strength athletes (15 studies). Differences in LVEDD were also reduced when measurements were corrected for BSA with values of 26 mm/m* in controls, 27 mm/m* in endurance athletes, and 28 mm/m* in resistance athletes. These observations minimized the group differences in cardiac morphology, and they also provided contradiction for the concept of sportspecific cardiac morphological changes because lower corrected LVEDD measurements were found in endurance athletes who engage in volumeoverload types of exercise training and who would be expected to show the greatest change in internal dimensions. Body surface area, however, does not account for differences in body composition. Independent of BSA, relationships have been reported between LV mass and lean body mass,27 suggesting that the degree of muscularity could be an important predictor of cardiac dimensions. To examine this relationship, we obtained Heath-Carter somatotype
characteristics as an index of mesomorphy or muscularity, ectomorphy or linearity, and endomorphy or adiposity in studies of echocardiographic LV dimension and BSA of 250 long-distance runners and road cycling racers. Regression analysis showed a significant positive relationship between 1VPW and the degree of mesomorphy or muscularity and, conversely, an inverse relationship between LVPW and the degree of ectomorphy.29 When additional anthropometric measurements of the torso were obtained in a subset of 40 endurance athletes, results from multiple regression analyses indicated that chest and rib circumferences and the degree of endomorphy accounted for approximately 50% of the variance of LVPW thickness, and that 80% of the LVPW variance could be explained with consideration of other anthropometric data, such as the axillary diameter, mesomorphy, and BSA. For LVEDD, the major contributors were BSA, systolic blood pressure, chest depth, and resting heart rate, which significantly accounted for 53% of the variance. A similar investigation probably should be repeated using a larger group of subjects and only selected anthropometric variables to minimize the overlapping effects of independent variables; however, the observations already demonstrated indicate the importance of considering body dimensions in studies of cardiac morphology. Results of correlative studies between parents and child, biological siblings, and pairs of monozygotic and heterozygotic twins also suggest a genetic influence30s31which could amount to 50% of the variance in cardiac dimensions.30 Illegal Drug Supplementation The influence of anabolic steroid use on cardiac dimensions needs to be considered. In animal models, anabolic drugs result in significant hypertrophy, ultrastructural alterations, and metabolic disturbances of the ventricular myocardium.32,33 In humans, there are only limited data on the influence of anabolic steroids or other illegal drug use on cardiac dimensions in athletes.34-36 In a comparison of body builders who reported a previous use of anabolic steroids for an average cycle length of 7 weeks with others who had never taken anabolic steroids, Salke et a1.34 reported no significant differences in LV wall and septal thickness, either in absolute terms or as corrected for BSA. However, a
The Athlete Heart
detailed account of the proportion of athletes who continued to take drugs at the time of the study was not provided. Similarly, an investigation of body builders before and after 6 weeks of taking testosterone, anabolic steroid, and human growth hormone (dosages not reported) demonstrated no significant differences in LVEDD, LVPW, or interventricular septal thickness.35 In contrast to this are the results of studies by Urhausen et a1.36in 14 body builders who took high doses of steroids for an average of 11 weeks during the previous 12 months and who were still using steroids or had only recently stopped them. Significantly higher absolute LV wall thickness was found in drug users than in nonusers. Similarly, 10 body builders who took high doses of anabolic steroids over 13 l/2 weeks showed significant increases in LVPW or interventricular wall thicknesses at the end of the steroid cycle. 37The influence of illegal drug supplementation on cardiac morphology of athletes has not been clearly established. The issue is complicated by the difficulty in obtaining accurate information about the administration of drugs, the exact type and proportions of drugs used, the duration of administration cycles, and the precise times of use and nonuse cycles.
CLINICAL
AND PHYSIOLOGICAL SIGNIFICANCE Echocardiographic Observations in Active Children Study of the “athlete heart” can provide guidelines for the physician to distinguish the big healthy heart from pathologic cardiomegaly. In active children and adolescents, the diagnosis of hypertrophic cardiomyopathy could be replaced by that of the”athlete heart” if the child is very active and regularity participates in sports. But investigations of cardiac dimensions in active children fail to clearly demonstrate an effect of regular physical activity. In an echocardiographic examination of champion childhood swimmers, Allen et al.% reported measurements of cardiac wall thickness greater than the 95th percentile of normal, with mean values of left atria1 and LV cavity size at the 5th percentile of normal. Follow-up studies as long as 15 years later in eight female and eight male swimmers, demon-
47
strated above normal cardiac volumes measured by chest roentgenograms in those who continued to train and normal volumes soon after the swimmers stopped training. 39 Differences in total blood volume, resting heart rate, and body composition were not considered. Moreover, in most recent investigations of trained and untrained 12-year-old boys and girls, matched for skeletal age and fat-free mass, no significant differences in LV internal diameter or posterior wall thickness were found.40*41This is compatible with observations of Blimkie et al.” showing a significant correlation between cardiac dimensions and body size in boys aged 10 to 15 years. The authors concluded that the significant correlation observed between cardiac dimensions and maximal aerobic power, a determining factor for aerobic performance, could be attributed mainly to the shared influence of body size on both factors. Upper Limits of Clinical Normality In an investigation of nearly 1000 athletes of national and international caliber competing in 25 different sport disciplines, echocardiographic cardiac dimensions were found to range from 44 mm to 66 mm (x 54.2 mm) for LVEDD and from 7 mm to 13 mm (x 10.4 mm) for LVPW.43 These measurements are similar to the average values summarizing cross-sectional echocardiographic studies (Figures 1 to 3). They indicate that even in athletes involved in rigorous physical training programs for several years, LV dimensions are not very different from normal subjects, with values usually within the expected clinical range. In fact, further data analysis showed that LVPW exceeded 13 mm in only 16 (1.7%) of the 1000 athletes- 15 rowers and one cyclist. As discussed previously, this could be related to the very large body build generally observed in rowers, but it could also be an association with the use of illegal drugs. Indeed, using this same upper limit, Urhausen et al.% found abnormal LVPW measurements in 11 of the 14 weight lifters who used steroids and in none of the nonusers. Although these observations do not provide a clear-cut definition for the diagnosis of true myocardial wall hypertrophy, they substantiate the finding that ventricular hypertrophy is not a condition common to the athlete. The clinical implication is that unless an individual is abnormally large or is a user of anabolic steroids, even the heart of a
Progress in Pediatric Cardi~lo~
48
very active child or adolescent of clinical normality. Physiologic
is within
the range
Significance
The limiting factor to maximal oxygen uptake has been sought for several decades. Because of significant correlations between measurements of LVEDD or LV mass and maximal oxygen uptake in athletes and nonathletes, it has been suggested that cardiac dimension limits the pumping capacity of the heart and, therefore, also limits maximal oxygen uptakea (and in Table 1 see, Zeldis et al., Bekaert et al., S’Jongers et al., Dickhuth et al., and Milliken et al.). However, this reasoning is difficult to accept on both methodological and theoretical grounds. First, computation of a significant correlation coefficient merely indicates that the variation in one parameter is affected by variations in the other. If training-induced changes in resting heart rate or plasma volume result in changing LVEDD, and training in turn increases maximal oxygen uptake, then these parameters should be statistically related. This does not mean, however, that resting LVEDD is the determining factor for maximal uptake. A significant correlation is also found between vital capacity and maximal oxygen uptake; however, pulmonary capacity has not been proposed as a limiting factor. It is also noteworthy that most of the reported correlations have been found only when maximal oxygen uptake measurements from both sedentary controls and endurance athletes were pooled, almost doubling the range of values of maximal uptake. Second, significant training-induced increases in maximal oxygen uptake have been reported without concomitant changes in LVEDD (Table 2). Conversely, in an investigation of masters and young endurance athletes, maximal oxygen uptake was found to be significantly lower in older athletes, although no differences were seen in resting LVEDD.” Finally, in rats, maximal oxygen uptake remained unchanged after cardiac enlargement was induced by isoproterenol administration.46 Thus,
if the cardiovascular
system limits maxi-
mal oxygen uptake, as suggested by relationships between oxygen delivery and maximal oxygen uptake, there is little evidence to indicate that the limiting factor is resting cardiac dimension. Moreover, recent studies suggest the involvement of several
factors rather than a single one.“Muscle mitochondrial enzyme levels, muscle capillarity, pulmonary alveolo-capillary exchanges, and central factors may be limiting factors, and the weakest link in one individual may not be the critical factor in another.
REFERENCES 1. Henschen SW. Sk&auf und skidwettlauf: eine medizinische sportstudie. In: Metteilungen aus der Medizinischen Klinik zu Upsala. Fischer Verlag; 1899: 1-74. 2. Morganroth J, Maron HJ, Henry WL, Epstein SE. Comparative ventricular dimensions, volumes and performance. Ann Intern Med. 1975;82:4-9. 3. George KP, Wolfe LA, Burggraf GW. The “athletic heart syndrome”: a critical review. Sports Med. 1991;11:300-311. 4. Maron BJ. Structural features of the athletic heart as determined by echocardiography. J Am Golf Cardiol. 1986;7:190-203. 5. Peronnet F, Ferguson RJ, Perrault H, Ricci G, Lajoie D. Echocardiography and the athlete’s heart. Physician Sports Med. 1981;9:102-112. 6. Feigenbaum H. Echocardiography. 4th ed. Philadelphia: Lea & Febiger; 1986. 7. McDicken WN. Diagnostic Ultrasonics: Principles and Use of Instruments. New York: J. Wiley & Sons; 1976. 8. Bing OWL, Matsushita S, Fanburg BL, Levine HL. Mechanical properties of rat cardiac muscle during experimental hypertrophy. Circ Res. 1971;28:234245. 9. Ross J Jr. Adaptations of the left ventricle to chronic volume overload. Circ Res. 1974;34(Suppl IIf:6470. 10. Sung R, Stephens M, Blayney L, Henderson A. Cardiac morphology and its regression in rat: comparison of morphological changes in response to aortic constriction, iron deficiency anemia and isoprenaline. J Mol Cell Cardiol. 1982;14:501-512. 11. Marcus ML, Eckberg DL, Braxmeir JL, Abboud FM. Effects of intermittent pressure loading on the development of ventricular hypertrophy in the cat. Circ Res. 1977;40:484-488. 12. Bennett DH, Evans DW, Raj MV. Ech~~dio~aphic left ventricular dimensions in pressure and volume overload. Their use in assessing aortic stenosis. Br Heart J. 1975;37:971-977. 13. Gray KE, Barritt DW, Ross FG. Echocardiographic assessment of severity of aortic regurgitation. Br Heart J. 1975;37:558. 14. De Maria AN, Neumann A, Schubart PJ, Lee G, Mason DT. Systematic correlation of cardiac cham-
The Athlete Heart
ber size and ventricular performance determined with echocardiography and alterations in heart rate in normal persons. Am 1 Cardiol. 1979;43:1-9. 15. Bungo MW, Goldwater DJ, Popp RL, Sandler H. Echocardiographic evaluation of space shuttle crew members. J Appl Physiol. 1987;62:278-283. 16. Katz R, Karline JS, Resnick R. Effects of a natural volume overload state (pregnancy) on left ventricular performance in normal human subjects. Circulation. 1978;58:434-441. 17. Rubler S, Damani PM, Pinto ER. Cardiac size and performance during pregnancy estimated with echocardiography. Am ] Cardiol. 1977;40:535-545. 18. Lewis BS, Lewis N, Gotsman M. Effect of standing and squatting on echocardiographic left ventricular function. Eur J Cardiol. 1980;11:405-412. 19. Nixon JV, Murray GR, Leonard I’D, Mitchell JH, Blomqvist CG. Effect of large variations in preload of left ventricular performance characteristics in normal subjects. Circulation. 1982;65:698-703. 20. Convertino VA, Brock PJ, Kell LC, Bernauer-Greenleaf JE. Exercise training-induced hypervolemia: role of plasma albumin, renin and vasopressin. J Appl Physiol. 1980;48:665-669. 21. Convertino VA. Blood volume: its adaptation to endurance training. Med Sci Sports Exer. 1991;23: 1338-1348. 22. Amon KW, Crawford MH. Upright exercise echocardiography. Clin Ultrasound. 1979;7:373-376. 23. Dickuth HH, Nause A, Staiger J, Bonzel T, Keul J. Two dimensional echocardiographic measurements of left ventricular volume and stroke volume of endurance trained athletes and untrained subjects. Int 1 Sports Med. 1983;4:21-27. 24. Martin WH III, Coyle EF, Bloomfield SA, Ehsani AA. Effects of physical deconditioning after endurance training on left ventricular dimensions and stroke volume. J Am Co11 Cardiol. 1986;7:982-989. 25. Epstein M, Goldberg SJ, Allen HD, Konecke L, Wood J. Great vessels, cardiac chamber and wall growth patterns in normal children. Circulation. 1975;67:1124-1129. 26. Henry WL, Gardin JM, Ware JH. Echocardiographic measurements in normal subjects from infancy to old age. Circulation. 1980;62:1054-1060. 27. Savage DD, Levy D, Dannenberg AL, Garrison RJ, Castelli WP. Association of echocardiographic left ventricular mass with body size, blood pressure and physical activity (the Framingham study). Am J Cardiol. 1990;65:371-376. 28. Hagan RD, Laird WP, Gettman LR: The problem of per-surface area and per-weight standardization indices in the determination of cardiac hypertrophy in endurance athletes. 1 Cardiopulm Rehabil. 1985; 5~554-560.
49
29. Perrault H, Peronnet F, Lebeau R, Nadeau R. Relationship between left ventricular morphological characteristics, maximal aerobic power and body composition. Can ]Appl Sport Sci. 1983;8:196. Abstract. 30. Bouchard C, Lortie G. Heredity and endurance performance. Sports Med. 1984;1:38-64. 31. Landry F, Bouchard C, Dumesnil J. Cardiac dimensions changes with endurance training: indications of a genotype dependency. JAMA. 1985;254:77-80. 32. Behrendt J, Boffin H. Myocardial cell lesions caused by anabolic hormone. Cell Tissue Res. 1977;lBl: 423-426. 33. Weicker H, Hagele H, Repp B, Kolb J. Influence of training and anabolic steroids on the LDH isozyme pattern of skeletal heart muscle fibers of guinea pigs. Int 1 Sports Med. 1982;3:90-96. 34. Salke RC, Rowland TW, Burke EJ. Left ventricular size and function in body builders using anabolic steroids. Med Sci Sports Exer. 1985;17:701-704. 35. Zuliani U, Bemadini B, Catapano A, Campana M, Cerioli G, Spatini M. Effects of anabolic steroids, testosterone and HGH on blood lipids and echocardiographic parameters in body builders. Int 1 Sports Med. 1989;10:62-66. 36. Urhausen A, Holpes R, Kindermann W. One- and two-dimensional echocardiography in body builders using anabolic steroids. Eur 1 Appl Physiol. 1989; 58~633-640. 37. Spiga L, Pesce G, Papagna D, Bavastro G, Odiglia G. Modificazione dei parametri ecocardiografici in body builders in trattmento con steroidi anabolizzanti. Med Sport. 1990;43:7-11. 38. Allen HD, Goldberg SJ, Sahn DJ, Schy N, Wojcik R. A quantitative echocardiographic study of champion childhood swimmers. Circulation. 1977;55: 142-195. 39. Rost R. The athlete’s heart. What we did learn from Henschen, what Henschen could have learned from us! 1 Sports Med Physical Fitness. 1990;30:339-346. 40. Telford RD, McDonald IG, Ellis LB, Chennels MHD, Sandstrom ER, Fuller PJ. Echocardiographic dimensions in trained and untrained 12-year-old boys and girls. 1 Sports Sci. 1988;6:49-57. 41. Auriacombe L, Mandel C, Fermont L, et al. Fonction ventriculaire gauche et adaptation cardiovasculaire a l’effort du jeune sportif. Arch Ma1 Coeur. 1987;4: 544-549. 42. Blimkie CJR, Cunningham DA, Nichol PM. Gas transport capacity and the echocardiographicallydetermined cardiac size in children. J Appl Physiol.
1980;49:994-999. 43. Pellicia A, Maron BJ, Sparato A, Proschan MA, Spirit0 P. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl
50
Progress in Pediatric Cardiology
J Med. 1991;324:295-301. 44. Pannier JL, Bekaert IE, Pennier R. Echocardiographic and radiographic study of cardiac dimensions in relation to aerobic work capacity. J Sports Med. 1982;22:165-171. 45. Heath GW, Hagberg JM, Ehsani AA, Holloszy JO. A physiological comparison of young and older endurance athletes. J Appl Physiol. 1981;51:634-640. 46. Baldwin KM, Ernst SB, Mullin WJ, Schrader LF, Herrick RE. Exercise capacity and cardiac function
of rats with drug-induced enlargement. J Appl Physiol. 1982;52:591-595. 47. Saltin B, Strange S. Maximal oxygen uptake: “old” and “new” arguments for a cardiovascular limitation. Med Sci Sports Exer. 1992;24:30-37. Note: Some of the references from Tables 1 and 2 are not included in the bibliography because of space constraints. A list of these references is available on request to the authors.
In 1897 Henschen’ used cutaneous percussion to examine the hearts of cross-country skiers and reported that those with larger hearts also had better placements in the race. Nearly 100 years later and after several hundred publications, the significance of this observation is still debated. The term, “athlete heart,” was introduced to describe the cardiovascular effects of exercise in competitive athletes. Two decades ago accurate direct in vivo measurements of cardiac structures became feasible for the first time with the introduction of echocardiography. Between 1975 and 1992, more than 80 studies compared left ventricular (LV) morphology in more than 1000 nonathletes and athletes with endurance or strength fitness (Table l), and 20 other studies examined the changes in LV structure of healthy sedentary individuals following predominantly endurance-type training programs (Table 2). The common interpretation of these observations is that regular physical activity induces cardiac hypertrophy . However, a large number of confounding factors have not been considered in the interpretation of these data. This paper will critically review the scientific literature concerning cardiac morphological adaptations to training in humans that suggests that athletes, in fact, may have rather “normal” cardiac dimensions. Address correspondence to Dr. Helene M. Perrault, Service de Cardiologie et de Medecine Pulmonaire, HBpital Ste-Justine, 3175 Chemin Cote Ste-Catherine, Montreal, Quebec, Canada, H3T lC5.
MORPHOLOGY OF THE ATHLETE HEART: REVIEW OF ECHOCARDIOCRAPHIC DATA Two different methodological approaches have been used in the echocardiographic examination of cardiac morphology. Studies with cross-sectional design have compared LV structures of athletes involved in different sport disciplines to those of sedentary “nonathletes,” whereas studies with longitudinal design have examined changes in these structures before and after several weeks or months of regular physical training. In most studies LV enddiastolic measurements have included internal diameter (LVEDD) and posterior wall thickness (LVPW), with interventricular septal wall thickness reported in only some cases. The results of a metaanalysis of findings from cross-sectional comparisons of sedentary controls to endurance- or strengthtrained athletes appear in Figures 1 and 2, respectively (see Table 1 for references). The average LV dimensions calculated from the reported group means in each study is shown as well as the weighted mean, calculated from the overall average of group means, weighted for the number of individual observations in each group. As seen in Figure 1, no difference can be observed between weighted means and group means of endurance athletes or their sedentary controls, reflecting the homogeneity in echocardiographic measurements of LV structures both in these athletes and in controls. Statistical analysis of the results indicates significant differences in LV morphological characProg Pediatr Cardiol 1993; 2(2):40-50 Copyright 0 1993 by Andover Medical
The Athlete Heart
TABLE
1. Cross-Sectional Echocardiographic
41
Studies of Athletes
Reference
Comparisons
N/Category
Morganroth et al. (1975) Rost et al. (1975) Lemon et ai. (1976) Nutter et al. (1976) Houdas et al. (1976) Roeske et a1. (1976) Falsetti et al. (1977) Fannapazir et al. (1982) Gilbert et al. (1977) Howald et al. (1977) Underwood et al. (1977) Laurenceau et al. (1978) Parker et al. (1978) Quiret et al. (1978) Zeldis et al. (1978) Grayevskaya et al. (1979) Ikaheimo et al. (1979) Monnet et al. (1979) Zoneraich et al. (1979) Adda et al. (1981) Blair et al. (1980) Cohen et al. (1980) Drescher et al. (‘1980) Lesbre et al. (1980) Longhurst et al. (1980) Nishimura et al. (1980) Kanakis et al. (1980) Bose et al. (1980) Bekaert et al. (1981) Fisher et al. (1981) Keul et al, (1981) Mumford et al. (1981) Paulsen et al. (1981) Rubal et al. (1981) Heath et al. (1981) Menapace et al. (1982) Snoeckx et al. (1982) Wieling et al. (1982) Fagard et al. (1983) Sugishita et al. (1983) Spirit0 et al. (1983) Child et al. (1984) Moore et al. (1984) Shapiro (1984) Shaviro and Mckenna (1984) . Cohen et al. (1985) Golan et al. (1985) Hauser et al. (1985) SJongers et al. (1985) Sparato et al. (1985) Wolfe et al. (1985) Csanady et al. (1986) Fargard et al. (1987) Van Den Brocke et al, (1988) Dickhuth et al. (1989) Fisher et al. (1989) Sepulveda et al. (1989) Percy et al. (1990)
C/E/R
16/15/14 10
; C/E R C/E E C/E C/E C/E C/E C/E C/E E E C/E C/E C/E C/E
26/20 1000 18 26120 818 10/20 12/11 15 25 31/152 13/12 32/28 20/12
C/E C/E C/E C/E/R C/E/R C/E
20/20 15130 75/21 -/20/10 10/12/17 35160
C/R
15/29 11/14
C/E R C/E/R C/E C/E C/E C/E C/R C/E E C/E C/E/R C/R C/E/R C/E C/E/R C/E C/E/R C/E/R C/E C/E C/E/R C/E E C/E C/R C/E C/E C/E
19/19 1018 10/9 18/32 10113 17131 23 12/12 14131/17 12/9/13 14114 40/104134 20/10 10/10/10 22111111 lo/11 501194/69 13/11 29 16/16 lO/lO 7/7 20122 14110
This table lists echocardiographic studies that have been considered in the computation of average LV dimensions found in sedentary controls (C), endurance athletes (E), and resistance- or power-trained athletes (R). When available, the number of controls, endurance, or resistance athletes examined is also shown.
Progress in Pediatric Cardiology
42
TABLE 2. Longitudinal Echocardiographic
Studies of Athletes
Reference
Type
Duration (weeks)
N/Category
Frick et al. (1970) Houdas et al. (1976) DeMaria et al. (1978) Ehsani et al. (1978) Wolfe et al. (1979) Michielli et al. (1979) Righetti et al. (1980) Teronnet et al. (1980) Perrault et al. (1982) Ricci et al. (1982) Wazana et al. (1980) Adda et al. (1981) Thompson et al. (1981) Wieling et al. (1981) Adams et al. (1985) Hickson et al. (1985) Wolfe et al. (1985) Cox et al. (1986) Younis et al. (1987) Rubal et al. (1987) Martin III et al. (1986)
E E E E E E E E E E/R E E E E E E E E E E D
8 28 11 9 24 14 10 20 20 8/20 52 11 11 28 14 10 30 7 24 10 3/8/12
20 15 24 8 15 14 18 11 14 8/20 26 11 10 23 50 12 12 11 19 10 6
This table presentsechocardiographicstudies that have been considered in the computation of average LV dimensionsbefore and after endurance(E) or resistance(R) training or after deconditioning (D). The duration of training is provided in the middle column.
ECHOCARDIOGRAPHIC “. 1375 endurance athletes SO
STUDIES
n-340
(19751991)
‘resistance”
athletes
and 255
controls
and 748 controls
1
LVEDD (mm)
Y
LVEODCmm)
LVPWCmm)
Heart
I
*,I?,. mean
Bsa Alill. weighted mean
0
cont. mean
lllwl
LVPWd (mm)
rate(bpm)
Cont. wsighted mean
Figure 1. Summary of the findings of cross-sectional designed echocardiographic studies conducted between 1975 and 1991, comparing LV dimensions of endurance athletes with nonathletic controls. Calculated means + standard deviations from all groups of athletes and controls are shown in filled and dotted bars. Weighted means, calculated according to the number of observations per group, are shown in diagonal and vertical hatched bars. *Statistical significance (F’ < .05) between athletes and controls.
1
LVEDDfSSA
I
Afhl. mean
@a
0
cant. mean
lllwn cont. Weighted mean
LVPWdIBSA
AthI. weighted mean
Figure 2. Summary of the findings of cross-sectional designed echocardiographic studies conducted between 7975 and 1991, comparing LV dimensions in resistance athletes with nonathletic controls. (A) Shows the calculated means f standard deviations for all groups of athletes and nonathletes in filled and dotted bars, as well as the computed weighted means in diagonal and vertical hatching. (B) Illustrates the calculated means _t standard deviations of LV dimensions, corrected for BSA in resistance athletes and nonathletes. Ytatistical significance (P < .05) between athletes and nonathletes.
The Athlete Heart
teristics between groups. The average dimensions calculated for LVEDD and LVPW in over 1200 endurance athletes are 53.5 f 3.4 mm and lo.2 f 1.5 mm, respectively, whereas those of some 800 age-matched controls are 48.2 f 2.2 mm and 8.66 f 1.1 mm. Calculated average resting heart rates were 55 + 5 bpm and 66 k 6 bpm, respectively, in athletes and controls. As first shown by Morganroth et a1.2 cardiac dimensions measured in resistance- or strength-trained athletes are different from those observed in endurance athletes, with mean LVEDD and LVPW calculations in a total of 340 athletes in 25 studies of 52.2 f 2.2 mm and 11.2 + 1.5 mm, respectively (Figure 2). The classification of some sports in terms of resistance or strength attributes is not as easily established as for pure endurance events. Consequently, classification designations are based frequently on an exclusion criteria of an endurance sport and include athletes from a number of various disciplines such as judo, shotput, discus throw, weight lifting, body building, and sprint running. The wide variation in the selection of subjects from one study to another may be seen in the differences observed between weighted and group means. Application of statistical analyses to the overall group means of endurance athletes, strength athletes, and controls indicate significant differences (p < .05) between groups, although the validity of the analysis may be questioned because of the inhomogeneity of variance between groups. A summary of the echocardiographic data from longitudinal investigations of healthy sedentary individuals is presented in Figure 3 (see Table 2). In all cases, values are comparable to those found in sedentary controls in the previous cross-sectional studies, with average values calculated in 257 subjects of 49.1 + 3.0 mm and 9.3 f 1.2 mm for LVEDD and LVPW. After 4 to 52 weeks of endurance training (average 18 weeks), the calculated average dimensions were 51.6 f 2.9 mm and 9.6 f 1.1 mm, showing statistically significant increases. No relationship, however, could be calculated between the training duration and the magnitude of change in LV dimensions. These data are not new. They merely provide an up-date of numerous earlier reviews.3-5 In the next section, however, several factors will be discussed that may have biased the interpretation of these studies. Three methodological problems and sev-
43
M
LONGITUDINAL
STUDIES
(29751990)
Figure 3. Comparisons of the LV free wall and cavity dimensions of sedentary individuals before training with measurements in sedentary controls from crosssectional designed studies (top), after training (middle), endurance athletes from cross-sectional studies (second from bottom), and resistance athletes from cross-sectional studies (bottom). The number of studies from which the mean values are calculated is shown by n.
era1 confounding factors of training need to be addressed.
METHODOLOGICAL
CONSIDERATIONS
Accuracy of the Measuring Tool One limitation of ultrasound measurements is axial resolution, the smallest distance between two structures that actually can be distinguished. Ultrasonic transducers generally used in adult echocardiographic studies have frequencies between 2.25 MHz and 3.0 MHz with an axial resolution of approximately 2.2 mm.6,7 However, in echocardiographic measurements of LVPW, differences between endurance athletes and controls (Table 1 references) range between 1.4 mm and 5.0 mm (average 1.6 mm). Similarly, after an endurance training program, pre- to posttraining differences in LVPW range from -0.6 mm to 1.0 mm (average change 0.34 f 0.46 mm) (Table 2 references). These differences remain below the limit of axial resolution of the echocardiographic technique. An aver-
Progress in Pediatric Cardiology
44
age difference of 5.5 mm (range 2.2 mm to 10.2 mm) is measured between the average LVEDD of athletes and controls, whereas pre- to posttraining differences range from 0.30 mm to 4.60 mm (average change 2.1 mm), at the limit of the resolution of the technique. It is important to appreciate that although statistical analyses provide a means to quantify the difference between group means, they do not indicate the theoretical or physiologic significance of the findings. Thus, for cardiac dimensions measured by echocardiography, statistically significant differences are meaningless unless they exceed the limit of axial resolution. Left Ventricular
Mass Index
The capacity for myocardial hypertrophy in response to systolic or diastolic pressure and volume overload has been well documented in animal models.8-11 In animals with aortic constriction, a significant increase (17%) in LV mass has been reported after 72 hours of aortic obstruction.8 Continuous LV volume overload was associated with an increase in mass of 14% after 1 week of application and an increase of 30% after 8 weeks.‘O In humans, ventricular hypertrophy can also be observed in response to conditions of continuous pressure or volume overload.“-l3 However, consider the extent of overload produced by physical training programs in humans. In most of the studies reviewed, the training programs consisted of moderate volume (endurance training) or pressure (strength training) overload for 1 hour and, exceptionally, 2 hours a day, 3 to 6 days a week for a total of 3 to 12 hours of exercise a week (Table 2). Yet changes in LV mass of approximately 30 % have been reported after only 2 weeks of training, corresponding to 6 or 8 hours of swimming (Ehsani et al. Table 2). Although it is tempting to conclude that this reflects a true myocardial hypertrophic response to training, other interpretations need to be considered. Left Ventricular
Volume
Left ventricular mass is calculated by subtracting values of internal LV volume from total LV volume, multiplied by specific gravity of cardiac muscle.6 Calculation of LV volume, in turn, relies on the assumption that the LV geometry is ellipsoidal, spherical, or cubic. In any of these models, computation of LV volume is based on the application of
a cubic function to the LV radius or the LVEDD. Depending on the equation used, differences from 15 % to 20% can be found in calculated LV volume, which limits the usefulness of such estimations of absolute LV volume. In addition, because of the cubed effect inherent in the computation of LV volume, small and nonsignificant differences in LV dimensions and measurement errors can become inflated, resulting in statistically significant differences. For example, consider the change in LV mass resulting from a l-mm increase in LVPW with no change in LVEDD. Although the basic change in LVPW with training is below the resolution of the measurement technique, a significant 15 % increase in “calculated” LV mass can be reported. This is not dissimilar to changes reported following endurance training, although an increase in LVEDD is usually also reported (Table 2). The question remains, however, as to whether this reflects a “true” increase in muscle mass.
CONFOUNDING FACTORS ASSOCIATED WITH LONGITUDINAL STUDIES By convention, the echocardiographic measurement of LVEDD is made in phase with the R wave of a simultaneously recorded electrocardiographic (ECG) tracing. This implies that changes in the R-R interval will affect the echocardiographic measurement of LVEDD. Similarly, changes in total blood volume caused by pharmacologic, pathologic, or physiologic conditions will affect it .i4-18Two factors associated with physical training, heart rate, and blood volume can affect LV diastolic filling and can change LVEDD without changing true LV mass. These are confounding factors associated with training, which should be taken into account in the interpretation of the echocardiographic data. Influence
of Sinus Node
Variability
The first confounding factor to consider is resting heart rate. Resting bradycardia is a well-known and widely accepted index of endurance training. In the present review of echocardiographic longitudinal studies, a difference of 11bpm is found between the average resting heart rates reported in endurance athletes and control subjects (Figure 3). Similarly, the echocardiographic examination of subjects following an endurance training program is associated with a significantly lower resting heart rate. The
The Athlete Heart
average change in heart rate calculated from the endurance training studies, reported in Figure 3, is 7 bpm. However, differences in resting heart rates have not been considered in the interpretation of echocardiographic measurements made after endurance training or in comparisons of endurancetrained athletes with sedentary controls. The effects of heart rate variations on LV internal diameter have been well documented. Using atria1 pacing, DeMaria et a1.14established an inverse linear relationship between LVEDD and heart rate, demonstrating that a IO-beat increment in resting heart rate is accompanied by a 2.7% decrease in LVEDD. Application of the prediction equation for LVEDD to the difference in resting heart rates in athletes and nonathletes (Figure 1) results in a difference of 1.4 mm in LVEDD. Similarly, according to the average calculated bradycardic response after endurance training studies, a l-mm increase in LVEDD could be predicted. Although this remains below the average change of 2.1 mm in LVEDD reported following training, these observations suggest that training bradycardia can account for a portion of the differences reported between endurance athletes and nonathletes following training. A regression analysis of the LVEDD and heart rates in 55 of the cross-sectional studies of athletes and controls indicates a significant correlation (r = 0.63) between these two variables. Efects of Endurance Training on Total Blood Volume Changes in the echocardiographic measurement of LVEDD have also been associated with changes in plasma volume or total blood volume, a second confounding factor. On retuning from an &day exposure to microgravity, space crew members showed a significant plasma volume contraction associated with a 23% decrease in echocardiographic determinations of LVEDD volume index.15 Conversely, significant increases in LVEDD have been reported following plasma volume expansion associated with pregnancy16st7 or after a change from upright to supine posture.18*19Chronic hypervolemia also occurs as a result of endurance training because of an increase in the total circulating plasma levels of electrolytes and proteins.20 Results from cross-sectional comparisons clearly indicate that endurance-trained athletes have 20% to 25% larger blood volumes than untrained subjects. Lon-
45
gitudinal studies of adaptations of blood volume to endurance training show that an increase can be measured after a single bout of exercise, and that a plateau is reached after only 1 week of training, with blood volume expansions ranging from 5% to 10% .21Similar increases in plasma volume with postural changes have been found to produce increases in LVEDD of up to 5 mm.22J3 Moreover, recent studies of highly trained athletes showed a S-mm decrease in the upright measurement of LVEDD after only 3 weeks of deconditioning, associated with a decrease in cardiac preload volume.24 Thus, the training effects on echocardiographic measurements of LVEDD are best explained by ventricular dilation due to training bradycardia and hypervolemia rather than by true eccentric cardiac hypertrophy. The argument against this view assumes that only stretching of the existing LV chamber without a concurrent increase in ventricular muscle mass results in a thinning of the wall, similar to that of a stretched balloon. However, from the equation for LV mass, it can be calculated that the difference in wall thickness produced by an increase in LVEDD of 2.2 mm (average change reported) without a change in LV mass would amount to a 0.5-mm decrease in LVPW, which essentially is too small to be detected by echocardiography.
CONFOUNDING FACTORS ASSOCIATED WITH CROSS-SECTIONAL COMPARISONS Cross-sectional LV echocardiographic measurements have also been used to indicate a direct effect of physical training on cardiac morphology. Although directional differences between trained and untrained subjects may be provided by such comparisons, they do not distinguish between the direct results of training and the effects of physical and physiologic factors. For example, differences in cardiac loading conditions from training-induced bradycardia or chronic hypervolemia have not been considered in the echocardiographic evaluations of endurance athletes, and cross-sectional design comparisons of measurements in athletes and nonathletes have often failed to consider the inffuence of anthropometric characteristics on cardiac dimensions.
46
Progress in Pediatric Cardiology
Body Dimensions The influence of body size on heart size is well documented. A number of early echocardiographic investigations in both children and adults6~25*26 and more recent results from the Framingham studyz7 have established significant correlations of LVEDD and LVPW with body surface area (BSA), body mass, and lean body mass. The influence of body size, however, was not considered in the interpretation of comparisons of cross-sectional echocardiographic cardiac dimensions in athletes and nonathletes. In athletes involved primarily in resistance-type and endurance-type training, initial comparisons led to the popular theory of sport-specific patterns of cardiac morphology. Results showed that resistance athletes had significantly larger LVPW (Figure 2) than that seen in endurance athletes, presumably because of the high pressure overload associated with their sport discipline. However, more recent study has shown (Fisher et al. Table l), that the difference in LVPW is greatly attenuated when values are corrected for BSA. In the compilation of results presented here, correction of LV dimensions reported in cross-sectional echocardiographic studies where BSA was either provided or could be calculated (Figure 2), resulted in corrected LVPW/ BSA values of 4.9 mm/m* in controls (26 studies), 5.6 mm/m2 in endurance athletes (35 studies), and 5.5 mm/m2 in resistance or strength athletes (15 studies). Differences in LVEDD were also reduced when measurements were corrected for BSA with values of 26 mm/m* in controls, 27 mm/m* in endurance athletes, and 28 mm/m* in resistance athletes. These observations minimized the group differences in cardiac morphology, and they also provided contradiction for the concept of sportspecific cardiac morphological changes because lower corrected LVEDD measurements were found in endurance athletes who engage in volumeoverload types of exercise training and who would be expected to show the greatest change in internal dimensions. Body surface area, however, does not account for differences in body composition. Independent of BSA, relationships have been reported between LV mass and lean body mass,27 suggesting that the degree of muscularity could be an important predictor of cardiac dimensions. To examine this relationship, we obtained Heath-Carter somatotype
characteristics as an index of mesomorphy or muscularity, ectomorphy or linearity, and endomorphy or adiposity in studies of echocardiographic LV dimension and BSA of 250 long-distance runners and road cycling racers. Regression analysis showed a significant positive relationship between 1VPW and the degree of mesomorphy or muscularity and, conversely, an inverse relationship between LVPW and the degree of ectomorphy.29 When additional anthropometric measurements of the torso were obtained in a subset of 40 endurance athletes, results from multiple regression analyses indicated that chest and rib circumferences and the degree of endomorphy accounted for approximately 50% of the variance of LVPW thickness, and that 80% of the LVPW variance could be explained with consideration of other anthropometric data, such as the axillary diameter, mesomorphy, and BSA. For LVEDD, the major contributors were BSA, systolic blood pressure, chest depth, and resting heart rate, which significantly accounted for 53% of the variance. A similar investigation probably should be repeated using a larger group of subjects and only selected anthropometric variables to minimize the overlapping effects of independent variables; however, the observations already demonstrated indicate the importance of considering body dimensions in studies of cardiac morphology. Results of correlative studies between parents and child, biological siblings, and pairs of monozygotic and heterozygotic twins also suggest a genetic influence30s31which could amount to 50% of the variance in cardiac dimensions.30 Illegal Drug Supplementation The influence of anabolic steroid use on cardiac dimensions needs to be considered. In animal models, anabolic drugs result in significant hypertrophy, ultrastructural alterations, and metabolic disturbances of the ventricular myocardium.32,33 In humans, there are only limited data on the influence of anabolic steroids or other illegal drug use on cardiac dimensions in athletes.34-36 In a comparison of body builders who reported a previous use of anabolic steroids for an average cycle length of 7 weeks with others who had never taken anabolic steroids, Salke et a1.34 reported no significant differences in LV wall and septal thickness, either in absolute terms or as corrected for BSA. However, a
The Athlete Heart
detailed account of the proportion of athletes who continued to take drugs at the time of the study was not provided. Similarly, an investigation of body builders before and after 6 weeks of taking testosterone, anabolic steroid, and human growth hormone (dosages not reported) demonstrated no significant differences in LVEDD, LVPW, or interventricular septal thickness.35 In contrast to this are the results of studies by Urhausen et a1.36in 14 body builders who took high doses of steroids for an average of 11 weeks during the previous 12 months and who were still using steroids or had only recently stopped them. Significantly higher absolute LV wall thickness was found in drug users than in nonusers. Similarly, 10 body builders who took high doses of anabolic steroids over 13 l/2 weeks showed significant increases in LVPW or interventricular wall thicknesses at the end of the steroid cycle. 37The influence of illegal drug supplementation on cardiac morphology of athletes has not been clearly established. The issue is complicated by the difficulty in obtaining accurate information about the administration of drugs, the exact type and proportions of drugs used, the duration of administration cycles, and the precise times of use and nonuse cycles.
CLINICAL
AND PHYSIOLOGICAL SIGNIFICANCE Echocardiographic Observations in Active Children Study of the “athlete heart” can provide guidelines for the physician to distinguish the big healthy heart from pathologic cardiomegaly. In active children and adolescents, the diagnosis of hypertrophic cardiomyopathy could be replaced by that of the”athlete heart” if the child is very active and regularity participates in sports. But investigations of cardiac dimensions in active children fail to clearly demonstrate an effect of regular physical activity. In an echocardiographic examination of champion childhood swimmers, Allen et al.% reported measurements of cardiac wall thickness greater than the 95th percentile of normal, with mean values of left atria1 and LV cavity size at the 5th percentile of normal. Follow-up studies as long as 15 years later in eight female and eight male swimmers, demon-
47
strated above normal cardiac volumes measured by chest roentgenograms in those who continued to train and normal volumes soon after the swimmers stopped training. 39 Differences in total blood volume, resting heart rate, and body composition were not considered. Moreover, in most recent investigations of trained and untrained 12-year-old boys and girls, matched for skeletal age and fat-free mass, no significant differences in LV internal diameter or posterior wall thickness were found.40*41This is compatible with observations of Blimkie et al.” showing a significant correlation between cardiac dimensions and body size in boys aged 10 to 15 years. The authors concluded that the significant correlation observed between cardiac dimensions and maximal aerobic power, a determining factor for aerobic performance, could be attributed mainly to the shared influence of body size on both factors. Upper Limits of Clinical Normality In an investigation of nearly 1000 athletes of national and international caliber competing in 25 different sport disciplines, echocardiographic cardiac dimensions were found to range from 44 mm to 66 mm (x 54.2 mm) for LVEDD and from 7 mm to 13 mm (x 10.4 mm) for LVPW.43 These measurements are similar to the average values summarizing cross-sectional echocardiographic studies (Figures 1 to 3). They indicate that even in athletes involved in rigorous physical training programs for several years, LV dimensions are not very different from normal subjects, with values usually within the expected clinical range. In fact, further data analysis showed that LVPW exceeded 13 mm in only 16 (1.7%) of the 1000 athletes- 15 rowers and one cyclist. As discussed previously, this could be related to the very large body build generally observed in rowers, but it could also be an association with the use of illegal drugs. Indeed, using this same upper limit, Urhausen et al.% found abnormal LVPW measurements in 11 of the 14 weight lifters who used steroids and in none of the nonusers. Although these observations do not provide a clear-cut definition for the diagnosis of true myocardial wall hypertrophy, they substantiate the finding that ventricular hypertrophy is not a condition common to the athlete. The clinical implication is that unless an individual is abnormally large or is a user of anabolic steroids, even the heart of a
Progress in Pediatric Cardi~lo~
48
very active child or adolescent of clinical normality. Physiologic
is within
the range
Significance
The limiting factor to maximal oxygen uptake has been sought for several decades. Because of significant correlations between measurements of LVEDD or LV mass and maximal oxygen uptake in athletes and nonathletes, it has been suggested that cardiac dimension limits the pumping capacity of the heart and, therefore, also limits maximal oxygen uptakea (and in Table 1 see, Zeldis et al., Bekaert et al., S’Jongers et al., Dickhuth et al., and Milliken et al.). However, this reasoning is difficult to accept on both methodological and theoretical grounds. First, computation of a significant correlation coefficient merely indicates that the variation in one parameter is affected by variations in the other. If training-induced changes in resting heart rate or plasma volume result in changing LVEDD, and training in turn increases maximal oxygen uptake, then these parameters should be statistically related. This does not mean, however, that resting LVEDD is the determining factor for maximal uptake. A significant correlation is also found between vital capacity and maximal oxygen uptake; however, pulmonary capacity has not been proposed as a limiting factor. It is also noteworthy that most of the reported correlations have been found only when maximal oxygen uptake measurements from both sedentary controls and endurance athletes were pooled, almost doubling the range of values of maximal uptake. Second, significant training-induced increases in maximal oxygen uptake have been reported without concomitant changes in LVEDD (Table 2). Conversely, in an investigation of masters and young endurance athletes, maximal oxygen uptake was found to be significantly lower in older athletes, although no differences were seen in resting LVEDD.” Finally, in rats, maximal oxygen uptake remained unchanged after cardiac enlargement was induced by isoproterenol administration.46 Thus,
if the cardiovascular
system limits maxi-
mal oxygen uptake, as suggested by relationships between oxygen delivery and maximal oxygen uptake, there is little evidence to indicate that the limiting factor is resting cardiac dimension. Moreover, recent studies suggest the involvement of several
factors rather than a single one.“Muscle mitochondrial enzyme levels, muscle capillarity, pulmonary alveolo-capillary exchanges, and central factors may be limiting factors, and the weakest link in one individual may not be the critical factor in another.
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The Athlete Heart
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49
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50
Progress in Pediatric Cardiology
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of rats with drug-induced enlargement. J Appl Physiol. 1982;52:591-595. 47. Saltin B, Strange S. Maximal oxygen uptake: “old” and “new” arguments for a cardiovascular limitation. Med Sci Sports Exer. 1992;24:30-37. Note: Some of the references from Tables 1 and 2 are not included in the bibliography because of space constraints. A list of these references is available on request to the authors.