Original Article
The Upper Limit of Physiologic Cardiac Hypertrophy in Highly Trained Elite Athletes
N Engl J Med 1991; 324:295-301January 31, 1991
- Abstract
- Abstract
Background.
In some highly trained athletes, the thickness of the left ventricular wall may increase as a consequence of exercise training and resemble that found in cardiac diseases associated with left ventricular hypertrophy, such as hypertrophic cardiomyopathy. In these athletes, the differential diagnosis between physiologic and pathologic hypertrophy may be difficult.
Methods.
To address this issue, we measured left ventricular dimensions with echocardiography in 947 elite, highly trained athletes who participated In a wide variety of sports.
Results.
The thickest left ventricular wall among the athletes measured 16 mm. Wall thicknesses within a range compatible with the diagnosis of hypertrophic cardiomyopathy (≥13 mm) were identified in only 16 of the 947 athletes (1.7 percent); 15 were rowers or canoeists, and 1 was a cyclist. Therefore, the wall was ≥13 mm thick in 7 percent of 219 rowers, canoeists, and cyclists but in none of 728 participants in 22 other sports. All athletes with walls ≥13 mm thick also had enlarged left ventricular end-diastolic cavities (dimensions, 55 to 63 mm).
Conclusions.
On the basis of these data, a left-ventricular-wall thickness of ≥13 mm is very uncommon in highly trained athletes, virtually confined to athletes training in rowing sports, and associated with an enlarged left ventricular cavity. In addition, the upper limit to which the thickness of the left ventricular wall may be increased by athletic training appears to be 16 mm. Therefore, athletes with a wall thickness of more than 16 mm and a nondilated left ventricular cavity are likely to have primary forms of pathologic hypertrophy, such as hypertrophie cardiomyopathy. (N Engl J Med 1991; 324:295–301.)
Media in This Article
Figure 1
Distribution of Maximal Left-Ventricular-Wall Thicknesses in the 947 Elite Athletes.Figure 2
Stop-Frame Two-Dimensional Echocardiograms Obtained during Diastole and Corresponding Schematic Drawings from a 21-Year-Old Cyclist with a Normally Thick Left Ventricular Wall and a 25-Year-Old Canoeist with Thickening of the Left Ventricular Wall.Article Activity
- Article
LONG-TERM athletic training produces the increases in the diastolic dimension of the left ventricular cavity, in the thickness of the left ventricular wall, and in the calculated left ventricular mass that make up what is commonly known as the "athlete's heart." 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 The increase in the thickness of the left ventricular wall is usually mild, but it may be more substantial in some athletes1 2 3 , 7 , 18 , 20 , 22 23 24 and create the diagnostic problem of distinguishing the physiologic hypertrophy of the athlete's heart from pathologic forms of hypertrophy, such as hypertrophic cardiomyopathy.18 This is an important differential diagnosis, since most instances of sudden death in athletes are probably due to hypertrophie cardiomyopathy.25 The distinction between these two forms of hypertrophy depends largely on the judgment of whether the magnitude of the left-ventricular-wall thickness exceeds that expected as a result of athletic training alone.
Precise definition of the physiologic limits on the extent to which cardiac dimensions, and in particular left-ventricular-wall thickness, can be altered by athletic conditioning has been hampered by a lack of echocardiographic data obtained systematically in large groups of highly trained athletes participating in a wide range of sports. We therefore assessed cardiac dimensions in a population of almost 1000 elite athletes who had trained over long periods, the majority of whom had attained international recognition for athletic achievement. This study population offered a unique opportunity to define the upper limit to which the thickness of the left ventricular wall may be increased by athletic training.
Methods
Selection of Subjects
The Institute of Sports Sciences, a division of the Italian National Olympic Committee, is responsible for the physiologic and medical evaluation of all amateur competitive athletes who form the Italian national teams from which Olympic athletes are selected every four years. Since 1960, in accordance with the statutes of the Italian Olympic Committee, it has been mandatory for all members of the junior and senior national teams to undergo a complete annual physiologic and medical evaluation. Since 1984, this evaluation has routinely included a history and physical examination, echocardiography, 12-lead and exercise electrocardiography, and chest radiography.
All the athletes evaluated in this program between September 1986 and August 1988 were initially included in our study population. Of the 958 athletes evaluated, 5 were subsequently excluded because of technically unsatisfactory echocardiograms. Six other athletes were excluded because of cardiovascular disease that necessitated their disqualification from competition; four of these had mitral-valve prolapse with ventricular tachyarrhythmias, and two had a bicuspid aortic valve with aortic regurgitation. Thus, the final study population comprised 947 athletes.
For athletes who had two or more echocardiographic examinations during the study period, the most recent echocardiogram was analyzed. Echocardiograms were obtained for each athlete during intense training; however, because of unavoidable practical considerations, echocardiography was not always performed with the athletes at the peak of their conditioning. All the athletes were judged to be free of systemic or cardiovascular disease, and blood pressure was consistently or predominantly less than 140/90 mm Hg.
Characterization of Study Subjects
The athletes participated in a range of 25 sports, which are listed in Table 1Table 2
Cardiac Dimensions as Assessed by Echocardiography in 738 Male and 209 Female Elite Athletes.*. Soccer, rowing, cycling, and track events had the most participants, reflecting the relative popularity, of these sports in Italy, as well as the fact that these are endeavors in which Italian athletes have traditionally achieved the most success in international competition. All the athletes had participated in vigorous training programs for competition, first at the youth level and subsequently at the national level, for periods ranging from 3 to 20 years. Of the 947 athletes, 480 had attained international recognition in competition, including 310 who participated in the Olympic games and 190 who were awarded medals for their performances in the 1987 or 1988 world championships or the 1988 Olympic games.The athletes ranged in age from 13 to 49 years (mean, 22); 738 (78 percent) were male, and 209 (22 percent) were female. They ranged in body-surface area from 1.43 to 2.39 m2 (mean, 1.90±0.1) (Table 1Table 1
Characteristics of 947 Elite Athletes, According to the Sports in Which They Participated.*).Echocardiography
Two-dimensional echocardiographic studies were performed with a commercially available Hewlett—Packard instrument (77020AC) with a 3.5-MHz transducer. Images of the heart were obtained in multiple cross-sectional planes, with the transducer in standard positions. The extent and distribution of hypertrophy were assessed from the two-dimensional echocardiogram, primarily in the parasternal long-axis and short-axis views, as described elsewhere.26 Diastolic left-ventricular-wall thickness was measured directly from the television monitor with the aid of calipers and a calibration scale produced by the instrument. Anterior ventricular septal thickness was assessed by an integrated analysis of the two-dimensional and the M-mode recordings. A particular effort was made not to include overlying trabeculations in measuring the thickness of ventricular septal and free walls.
The M-mode echocardiograms were derived from the two-dimensional images under direct anatomical visualization and were recorded at 100 mm per second. The thickness of the left ventricular wall and the dimensions of the left ventricular and left atrial cavities were measured on the M-mode echocardiograms according to the recommendations of the American Society of Echocardiography.27 Measures of left ventricular diastolic filling were obtained with Doppler echocardiography, as described elsewhere.28 , 29
The focus of this study was to determine the frequency with which athletes undergoing intense training may have left-ventricular-wall thicknesses within a range compatible with the diagnosis of hypertrophic cardiomyopathy. Therefore, we chose a cutoff value of ≥13 mm for wall thickness; this value clearly exceeds the 95 percent confidence limits (relative to body-surface area) for a normal nonathletic population similar in age to our athletes30 and falls within a range compatible with the diagnosis of hypertrophie cardiomyopathy.31 32 33 Other cardiac dimensions in the athletes were compared with available normal standards based on body-surface area and age.30
Left ventricular mass was calculated from end-diastolic wall thickness and cavity dimension, with appropriate correction for measurements obtained according to the recommendations of the American Society of Echocardiography.34 The left-ventricularmass index was calculated by dividing mass by body-surface area.35
Reproducibility
Variability between observers in the measurement of left-ventricular-wall thickness was assessed in a subgroup of 60 athletes by two investigators who measured wall thickness independently and without knowledge of the identity of the subjects. We chose 50 athletes from the master list of 947 athletes by selecting every 20th subject studied. The 10 remaining athletes were selected from among those on the same list who had a left-ventricular-wall thickness ≥13 mm.
Statistical Analysis
Data were expressed as means ±SD. Differences between means were assessed by the unpaired or paired Student's t-test, as appropriate. In the overall study population of 947 athletes, a multivariate linear model was used to assess the relation between the thickness of the left ventricular wall as a dependent variable and body-surface area, age, sex, and type of sport as independent variables.36 A two-tailed P value of ≥0.05 was considered to indicate statistical significance.
Results
Cardiac Dimensions in the Overall Study Group
The cardiac dimensions in the 947 subjects were largely typical of highly conditioned athletes18 (Tables 1 and 2). Their left ventricular end-diastolic dimensions ranged from 40 to 66 mm (mean, 52) and exceeded the normal value for a nonathletic population (≤54 mm) in 363 athletes (38 percent), including 38 in whom the dimension was ≥60 mm. Ventricular septal thickness ranged from 6 to 16 mm (mean, 9.7), and the thickness of the posterior left ventricular free wall ranged from 6 to 13 mm (mean, 9.1).
Athletes with Left-Ventricular-Wall Thickness ≥13 mm
Wall Thickness
Of the 947 athletes, only 16 (1.7 percent) were found to have a left-ventricular-wall thickness within a range compatible with the diagnosis of hypertrophie cardiomyopathy (≥13 mm)31 32 33 (Fig. 1Figure 1
Distribution of Maximal Left-Ventricular-Wall Thicknesses in the 947 Elite Athletes., 2Figure 2Stop-Frame Two-Dimensional Echocardiograms Obtained during Diastole and Corresponding Schematic Drawings from a 21-Year-Old Cyclist with a Normally Thick Left Ventricular Wall and a 25-Year-Old Canoeist with Thickening of the Left Ventricular Wall., and 3Figure 3
Stop-Frame Two-Dimensional Echocardiograms Obtained during Diastole from Two Elite Athletes, with Corresponding Schematic Drawings. and Table 3Table 3
Echocardiographic Findings in 16 Elite Male Athletes with the Most Marked Left Ventricular Thickening.*). The 16 athletes ranged in age from 18 to 27 years (mean, 22.5); all were men. Fifteen of the 16 were rowers or canoeists, and 1 was a cyclist. Wall thicknesses of ≥13 mm were observed in the anterior septum in three athletes (Fig. 2C and 2D), in the posterior septum in four (Fig. 3A), in both the anterior and posterior portions of the septum in six, and in both the septum and the free wall in three. The overall thickness of the left ventricular wall was quite uniform, however, since the thickness of one segment was never more than 2 mm greater than that of the contiguous segments.Three other athletes (two cyclists and one rower) had substantial left ventricular hypertrophy only at the apex (range, 15 to 18 mm) (Fig. 3B). In addition, 2 of the 16 athletes with wall thicknesses ≥13 mm in the basal portions of the left ventricle also had apical hypertrophy (of 15 and 18 mm).
Of the 209 female athletes in this study, most participated in highly demanding sports, such as track, swimming, skiing, and the pentathlon (a total of 80 athletes) or rowing, canoeing, and cycling (26 athletes). However, each of these 209 female athletes had a left-ventricular-wall thickness ≥11 mm.
Other Cardiac Dimensions
Each of the 16 athletes with a left-ventricular-wall thickness ≥13 mm had an end-diastolic left-ventricular-cavity dimension > 54 mm (range, 55 to 63) (Fig. 2C and 2D and Table 3). In 15 of these 16 athletes, the calculated left-ventricular-mass index exceeded the values reported in a normal population34; the aortic-root dimension exceeded normal values in 5 athletes (range, 37 to 39 mm). In all 16 athletes, the percentage of fractional shortening and left atrial dimension were within normal limits.
Determinants of Wall Thickness
In the overall study population of 947 athletes, a multivariate linear model was used to assess the relation between left-ventricular-wall thickness and body-surface area, age, sex, and type of sport. After multivariate adjustment, a significant association was found between wall thickness and each of these variables (P<0.0001). Specifically, wall thickness was independently associated not only with body-surface area, age, and male sex, but also with certain sports (i.e., rowing, canoeing, and cycling).
Left Ventricular Filling
Indexes of left ventricular diastolic filling obtained with Doppler echocardiography28 , 29 , 37 were within normal limits28 in 15 of the 16 athletes with a left-ventricular-wall thickness 3=13 mm; in the remaining athlete, the early and late diastolic peak velocities were both increased. The mean values for Doppler diastolic indexes in this group of athletes were as follows: peak early diastolic flow velocity, 69±12 cm per second; peak flow velocity during atrial systole, 30±8 cm per second; ratio of early to late peaks of flow velocity, 2.2±0.4; and slope of the descent of the early diastolic peak, 501 ±84 mm per second squared.
Athletic Achievement
As a group, the 16 athletes with a left-ventricular-wall thickness ≥13 mm appeared to be particularly successful with regard to their athletic achievements; 8 (50 percent) had been awarded medals for their performance at either the Olympic games or the world championships, and each of the remaining 8 athletes had been a medalist at other major international events, the Italian champion in his sport, or both. It is noteworthy that six athletes who substantially reduced their training for 40 to 240 days (mean, 90) after participation in the 1988 Olympic games had significant decreases in the thickness of the left ventricular wall. In these six athletes (Athletes 2, 7, 8, 11, 14, and 16 in Table 3), blind readings of serial echocardiograms obtained during peak training and after deconditioning showed decreases in wall thickness from 13.8±0.9 mm to 10.5±0.4 mm (P<0.002).
Electrocardiography
Electrocardiograms were within normal limits in 9 of the 16 athletes with a left-ventricular-wall thickness ≥13 mm.38 The other seven athletes had electrocardiographic alterations — precordial-lead voltages ≥30 mm in three, mild T-wave inversion in three, and first-degree atrioventricular block (0.26 second) in one. Electrocardiograms were normal in the three athletes with left ventricular hypertrophy confined to the apex.
Variability between Observers
Left-ventricular-wall thickness in 60 athletes ranged from 8 to 15 mm (mean, 10.2±1) as measured by the first observer, and from 8 to 15 mm (mean, 11.0±1) as measured by the second observer. The mean difference between observers was 0.8±0.7 mm. In each instance, there was agreement between the observers about which left ventricular segments had the maximal wall thickness.
Discussion
Previous echocardiographic studies have consistently demonstrated that trained athletes have a larger calculated left ventricular mass than sedentary normal controls of similar age and body size.1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 The greater left ventricular mass observed in athletes is due mainly to the presence of a larger left ventricular cavity, whereas the thickness of the left ventricular wall is usually similar to that in nonathletic controls.18 In some highly trained competitive athletes without apparent structural heart disease, however, the left ventricular wall may be substantially thicker than normal1 2 3 , 7 , 18 , 20 , 22 23 24 and may resemble that of some patients with hypertrophic cardiomyopathy.18 The critical importance of distinguishing the athlete's heart from hypertrophic cardiomyopathy becomes evident when one considers that this cardiac disease is probably the most common cause of sudden death in young athletes.25 This differential diagnosis is largely based on whether the thickness of the left ventricular wall exceeds that expected to be associated with athletic training. However, the upper limits to which left-ventricular-wall thickness may be increased by athletic training remain unknown, since most previous echocardiographic studies have focused on mean values for cardiac dimensions in relatively small groups of athletes.10 11 12 13 14 15 16 , 18 , 21
In an effort to clarify the diagnostic ambiguities between a physiologic increase in the thickness of the left ventricular wall and pathologic hypertrophy, we have defined the upper limit for left-ventricular-wall thickness in a population of almost 1000 elite athletes undergoing systematic and intense training. The highest value for wall thickness identified in our study population was 16 mm. In addition, a wall thickness compatible with a diagnosis of hypertrophie cardiomyopathy (≥13 mm) proved to be particularly uncommon; it was identified in less than 2 percent of our athletes. Moreover, this extreme morphologic expression of the athlete's heart appeared to be virtually confined to athletes training in rowing sports, since 15 of the 16 athletes with wall thicknesses of this magnitude were either rowers or canoeists and the 16th was a cyclist. Of more than 700 athletes participating in 22 other sports, none had a wall thickness ≥13 mm.
The greater left-ventricular-wall thickness we observed in many rowers and canoeists may have been due in part to the particularly rigorous and demanding training required by these sports at the elite level. In addition, these athletes, while working against high resistance, generate greatly increased cardiac output by performing a combination of isotonic and isometric exercise that involves both the arms and the legs. Indeed, our multivariate analysis showed that participation in a rowing sport was independently associated with wall thickness after adjustment for body size, age, and sex.
The findings of this investigation provide important new elements for the differential diagnosis between a physiologic increase in left-ventricular-wall thickness that is due to athletic training13 , 18 and hypertrophic cardiomyopathy.18 , 32 None of our 947 highly trained athletes, for example, had a wall thickness of more than 16 mm. Therefore, it can be inferred that a left-ventricular-wall thickness in excess of 16 mm, even in a highly trained athlete, is likely to represent a pathologic form of hypertrophy, such as hypertrophic cardiomyopathy. In addition, a left-ventricular-wall thickness ≥13 mm (which is compatible with the diagnosis of hypertrophic cardiomyopathy) was very uncommon and virtually confined to athletes training in the sports of rowing, canoeing, and occasionally cycling. Therefore, should a wall thickness of this magnitude be identified in athletes participating in other sports, it would probably represent pathologic hypertrophy. Each of our 16 elite athletes with a left-ventricular-wall thickness that would be compatible with the diagnosis of hypertrophie cardiomyopathy had an enlarged end-diastolic cavity (dimensions, 55 to 63 mm) — undoubtedly a manifestation of athletic training.18 This finding itself may be sufficient to distinguish most athletes with physiologic hypertrophy in this study from patients with hypertrophie cardiomyopathy, since in this disease the left ventricular cavity size is almost invariably normal or reduced (i.e., smaller than 55 mm).32 Furthermore, in our athletes with very thick walls the contours of the left ventricular wall were relatively smooth, whereas contiguous segments of the wall often show marked differences in thickness in patients with hypertrophie cardiomyopathy.31 , 32
Our study population comprised more than 200 female athletes, most of whom participated in highly demanding sports and 26 of whom competed in rowing, canoeing, or cycling. Nevertheless, each of these women had a left-ventricular-wall thickness ≥ 11 mm. This observation suggests that in female athletes, the increase in left-ventricular-wall thickness associated with intense training virtually never leads to wall thicknesses within a range compatible with the diagnosis of hypertrophie cardiomyopathy.
We consider it very unlikely that any of our athletes with wall thicknesses 3=13 mm had hypertrophic cardiomyopathy. None of them had other features suggestive of this disease,32 such as a family history of hypertrophic cardiomyopathy or sudden death, cardiac symptoms on exertion, evidence of dynamic subaortic obstruction, or an abnormal pattern of left ventricular filling.28 In addition, six athletes who reduced their training substantially for an average of 90 days after participation in the 1988 Olympic games had significant decreases in left-ventricular-wall thickness after deconditionine, a finding consistent with the known effects on physiologic hypertrophy of a reduction in training.5 , 15 , 18 , 19
An unexpected finding was that 3 athletes (not included among the 16 with a wall thickness ≥13 mm) had prominent hypertrophy confined to the left ventricular apex. Although this distribution of hypertrophy resembled that of patients with apical hypertrophic cardiomyopathy,39 40 41 each of these athletes had a normal electrocardiogram without the marked T-wave inversion frequently described in such patients.39 Therefore, the implications of the apical hypertrophy identified in a small number of our athletes remain uncertain.
It should be pointed out that populations of athletes may have important differences with respect to genetic, racial, or ethnic characteristics, as well as to the intensity, duration, and nature of their training program,18 and all these variables may theoretically influence cardiac dimensions. The athletes who constituted our study population were relatively homogeneous with regard to genetic and racial composition. In addition, certain sports with high levels of participation in the United States (such as football and basketball) were not represented, whereas participants in several other sports that are more popular in Europe (soccer, rowing, and cycling) made up a sizable proportion of the study population. Consequently, the athletes in the present study are not necessarily representative of all possible populations of highly trained athletes. Therefore, our findings should be used with some caution in the evaluation of individual athletes of different ethnic origin and also of athletes training in sports other than those we studied.
The determinants of performance in competitive athletes are numerous and complex, and their precise definition is well beyond the scope of this investigation. It is of interest, however, that of the 16 rowers, canoeists, and cyclists who had the thickest left ventricular walls, each demonstrated a remarkably high level of achievement in his sport, and 8 were among the top three competitors in the world in that sport. We do not know precisely how the thickness of the left ventricular wall may be related to the level of athletic performance. It is possible that an athlete's capacity or genetic predisposition to increase left-ventricular-wall thickness as a consequence of training may in some way reflect his or her ability to train more intensely and attain higher levels of achievement in competition.
Supported in part by the Italian National Olympic Committee.
We are indebted to Drs. Alessandro Biffi, Giovanni Caselli, and Maristella Granata for their important contributions and support.
Source Information
From the Institute of Sports Science, Department of Medicine, Comitato Olimpico Nazionale Italiano, Rome (A.P., A.S.); and the Cardiology Branch (B.J.M., P.S.) and the Biostatistics Research Branch (M.A.P.), National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md. Address reprint requests to Dr. Pelliccia at the Institute of Sports Science, Department of Medicine, Via dei Campi Sportivi, 46, 00197 Rome, Italy.
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