ventricular adaptation to physical exercise in elite ... physical exercise, the increase in the ventricular cavities should be .... measured at three sites (T 1,3,5).
European Heart Journal (1999) 20, 309–316 Article No. euhj.1998.1197, available online at http://www.idealibrary.com on
An echocardiographic study of right and left ventricular adaptation to physical exercise in elite female orienteers E. Henriksen*, J. Landelius†, T. Kangro*, T. Jonason*, P. Hedberg*, L. Wessle´n‡, C. N. Rosander‡, C. Rolf§, I. Ringqvist* and G. Friman‡ *Department of Clinical Physiology and Department of Research, Central Hospital, Va¨stera˚s; †Department of Clinical Physiology, ‡Department of Infectious Diseases, Uppsala University Hospital Uppsala; §Section of Sports Medicine, Department of Orthopaedic Surgery, Huddinge Hospital, Karolinska Institute, Stockholm, Sweden
Background A considerable body of echocardiographic studies has described how athletic training induces morphological adaptation of the left ventricle in male endurance athletes, but only a few studies have described left ventricular adaptation in female endurance athletes. In contrast to changes in the left ventricle far less attention has been directed towards right ventricular changes due to extensive physical exercise. The purpose of this study was to obtain normal values and to determine if there are any differences in right and left ventricular cavity and wall dimensions between female orienteers and females with a mainly sedentary lifestyle. Methods Echocardiography was performed in 42 highly trained elite female orienteers and 32 healthy female students with a predominantly sedentary lifestyle. The 74 females had no history of cardiac disease, a normal electrocardiogram and showed no echocardiographic abnormalities. M-mode and two-dimensional measurements of the right and left ventricular cavity and wall were obtained in elite orienteers and sedentary females. For the right ventricle and wall, multiple cross-sections were used and
Introduction A considerable body of echocardiographic studies has described how athletic training induces morphological adaptation of the left ventricle in male endurance athletes[1–5]. In contrast, there are only a few studies describing left ventricular adaptation in female endurance athletes[6]. Moreover, in contrast to changes in the left ventricle, far less attention has been directed towards right ventricular changes due to extensive physical Revision submitted 14 April 1998, and accepted 3 July 1998. Correspondence: Dr Egil Henriksen, Department of Clinical Physiology, Central Hospital, S-72189 Va¨stera˚s, Sweden. 0195-668X/99/040309+08 $18.00/0
measurements were obtained from the right ventricular inflow and outflow tract. Results The left ventricular end-diastolic cavity dimension and the left ventricular wall thickness were significantly greater in the athletes compared with the sedentary controls. The right ventricular inflow tract measurements were all significantly greater in the orienteers compared with the controls but the right ventricular outflow tract measurements were comparable in the study groups. The right ventricular wall thickness, calculated as the mean of three different wall measurements was an average of 13% greater in the athletes compared with the sedentary controls. Conclusion This study suggests symmetrical cardiac enlargement with a concomitant increase in both the right and left ventricular wall, probably reflecting the increased haemodynamic loading in the female athletes. (Eur Heart J 1999; 20: 309–316) Keywords: Echocardiography, female athletes, right and left ventricular measurements.
exercise[5,7]. This neglect may partly be explained by the complex nature of right ventricular cavity, the thin trabeculated right ventricular wall and its position beneath the sternum making imaging, measurements and functional assessment much more complex compared with the left ventricle. The present study was designed to examine the hypothesis that because both the left and the right ventricle are exposed to a large increase in haemodynamic loading during extensive and prolonged physical exercise, the increase in the ventricular cavities should be symmetrical with an increase in both the right and the left ventricular wall thickness. Two-dimensional and M-mode echocardiography were used to describe 1999 The European Society of Cardiology
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the structural cardiac changes caused by heavy training in female elite orienteers. This paper describes both right and left cardiac adaptation due to training.
Subjects and methods Study population Sixteen cases of sudden unexpected cardiac deaths occurred among young Swedish orienteers between 1979 and 1992; of these 15 were males and one was female[8]. An analysis showed that the death rate was increased among male elite orienteers but not among female orienteers[8]. However, both male and female elite orienteers in Sweden underwent an echocardiographic examination as part of an in-depth medical examination. The female orienteers were all highly trained endurance athletes, the majority attending special schools for talented orienteers. Some of the athletes were members of the senior or junior national team. From a group of 43 female athletes, we included the athletes with a normal electrocardiogram at rest and no echocardiographic evidence of heart disease. One subject was excluded because of hyperthyreosis. No one was excluded for other reasons. Thus a total of 42 female athletes comprised the final study sample. Some of the athletes had been elite performers for only a few years, whereas others for as long as a decade. Among the youngest female orienteers, the training load had been about 300–500 h of running each year and among the older orienteers demonstrating the highest performance, the training load had been up to 600 h of running, predominately in forest terrain, each year. Because of the increased death rate in the male orienteers, both the male and the female orienteers were recommended to decrease their training intensity and training load during the 6 months of the present investigation. However, we do not know to what extent each athlete followed these recommendations. All elite competitions were cancelled during this period. A group of 32 volunteer female students served as controls. It was determined that they all had a largely sedentary lifestyle and no one was a competitive athlete. They all had a normal ECG at rest and a normal echocardiogram and no one had history of cardiac disease. No one was a habitual smoker.
recordings were obtained for each subject. Three echocardiographers at one laboratory performed the examinations. One observer performed all the measurements and each parameter value was averaged over three cardiac cycles. All individuals were studied in the left lateral recumbent position and the echocardiograms were recorded in the standard parasternal and apical views. In the cross sections of the right ventricle, we used a low gain setting and special care was taken to be certain that the correct cross-sections were obtained.
M-mode measurements Left ventricular, aorta and left atrial dimensions were obtained based on the standards of the American Society of Echocardiography[9].
Two-dimensional measurements The two-dimensional measurements of the right and left cavity and wall dimensions were measured from the leading edge to leading edge principle and the right ventricular wall from the epicardial to the endocardial signal. When the ultrasound beam was parallel to the wall, the endocardial echo may spread. In these cases, we used the mid-point of the endocardial echo as the measurement point. All ventricular measurements were made from end-diastolic frames defined as the frame closest to the onset of the QRS complex. Imaging quality was graded on a three-point scale, where 1 indicated poor quality, 2 acceptable quality and 3 good quality. Grade 1 automatically eliminated the registrations from further analysis. Right ventricular (RV) cavity and free wall measurements were obtained according to the protocol of Foale et al.[11] (Fig. 1). From the inflow tract (IT) we selected RVIT 1-2-3; from the outflow tract(-OT) RVOT 1-3-4 was selected; and from the right ventricular chamber RV 1 and RV b were selected. Right ventricular wall thickness (T) was measured at three sites (T 1,3,5). Left and right atrial dimensions were measured at the end of ventricular systole, guided by carefully advancing the frames from the video recording using the mitral valve opening as guidance.
Intra-observer measurements Echocardiography Examinations were performed by using an Acuson XP 128 system (San Jose´, U.S.A.) with 2·5 or 3·5 MHz transducers. An ECG was recorded simultaneously and all examinations were stored on video-tapes for subsequent analysis. Measurements and recordings were made during normal breathing at end expiration. Colour flow mapping and pulsed and continuous wave Doppler Eur Heart J, Vol. 20, issue 4, February 1999
Intra-observer variability for M-mode and twodimensional measurements have previously been described in our laboratory[5].
Statistical analysis Absolute measurements and measurements corrected for body surface area were calculated and expressed as
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T1
311
RV
RVOT 1 RVIT 1
AO LV LA
RVA 1 RA Parasternal long-axis view of the right ventricular outflow tract
Parasternal long-axis view of the right ventricular inflow tract T3
T5
RVOT 3 RVOT 4
PA RA
PA LV
LA
Parasternal short-axis view of the aortic root
Right ventricular outflow view
RVb
RVIT 2 RV
RV 1
LV
LV 1
RVIT 3
LVIT 3 RA 1 RA b
Parasternal short-axis view of the tricuspid valve
LVb
LA 1 LA b
Apical 4-chamber view
Figure 1 Definitions of two-dimensional cavities, wall measurements and abbreviations. Right ventricle and atrium: RVOT 1, from the anterior right ventricular wall to the right ventricular septum; RVOT 3, just beneath the pulmonary valve annulus; RVOT 4, maximum distance between the anterior aortic wall and the right ventricular free wall; RVIT 1, one third of the distance below the annulus towards the region of the right ventricular apex; RVIT 2, the maximum perpendicular distance between the right side of the mid-interventricular septum to the right ventricular free wall; RVIT 3, within one third of the distance below the tricuspid valve annulus towards the right ventricular apex; RVA 1, the atrioventricular junction to which the anterior and posterior tricuspid leaflets attach; RV 1, from the right ventricular apex to the mid-point of the tricuspid valve annulus; RV b, in the middle third of the right ventricle; RA 1, the maximal diameter from the tricuspid valve annulus to the cephalic atrial wall. RA b, the maximal transverse atrial diameter. Left ventricle and atrium: LVIT 3, within one third of the distance below the mitral valve annulus towards the left ventricular apex; LV 1, from the left ventricular apex to the mid-point of the mitral valve annulus; LV b, in the middle third of the left ventricle; LA 1, the maximal diameter from the mitral valve annulus to the cephalic atrial wall; LA b, the maximal transverse atrial diameter; LVOT, just beneath the aortic valve from the left ventricular septum to the anterior mitral leaflet (early systole). RV=right ventricular; -OT=outflow tract; -IT=inflow tract; -A1=annulus; -b=short axis; -1=long axis; RA=right atrium; -b=short axis; -1=long axis; T=right ventricular wall thickness; LV=left ventricular; -OT=outflow tract; -IT=inflow tract; -b=short axis; -l=long axis; PA=pulmonary artery.
mean values and 95% confidence limits of the mean. Standard deviation (SD) was also calculated for each measurement. Intra-observer variability was expressed as the coefficient of variation between measurements.
Comparison between two measurements was made using 95% confidence limits of the mean and differences were considered statistically significant when the confidence limits of the mean did not overlap. Eur Heart J, Vol. 20, issue 4, February 1999
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Table 1 General characteristics of the 42 female elite orienteers and the 32 sedentary female controls Female orienteers MV95% CI* Age (years) Height (cm) Body mass (kg) Body surface area (m2) Heart rate (beats . min 1)
19·70·7 1691·6 57·61·6 1·650·03 563·0
SD
Sedentary controls
Range
MV95% Cl*
2·4 17–27 5·1 159–181 5·0 47–70 0·09 1·501·90 9·5 42–84
SD
24·41·2 1662·4 61·03·4 1·700·05 643·2
Range
3·3 17–30 6·7 149–180 9·3 48–85 0·14 1·402·00 8·6 43–80
*Mean value and 95% confident limits of the mean. Body surface area calculated according to Du Bois.
Table 2 Two-dimensional and M-mode echocardiography: left ventricular and left atrial dimensions in 42 female elite orienteers and 32 sedentary female controls. (Absolute measurements in mm) Female orienteers
M-mode measurements Ao LA IVS LVPW LVDd LVDs 2-dimensional measurements Left ventricular chamber LV b LV 1 Left ventricular outflow tract LVOT Left ventricular inflow tract LVIT 3 Left atrium LA 1 LA b
Sedentary female controls
MV95% CI*
SD
n
MV95% CI*
SD
n
25·60·6 35·11·0 10·00·4 9·20·3 48·50·8 30·70·9
1·7 2·8 1·1 1·0 2·6 2·8
34 34 42 42 42 42
25·60·8 34·11·2 8·30·3 7·40·2 46·61·1 29·81·1
2·0 3·1 0·8 0·5 3·4 3·4
29 28 32 32 32 32
36·11·0 84·52·0
3·0 6·1
39 40
33·21·1 81·02·2
2·8 5·8
30 30
21·10·4
1·2
42
20·50·6
1·5
32
42·91·0
3·2
40
40·41·3
3·4
30
48·31·6 38·81·3
4·7 3·9
37 37
46·31·8 36·31·3
4·6 3·3
29 37
*Mean value and 95% confidence limits of the mean. Two-dimensional measurements; see text and Fig. 1 for measurements and abbreviations. M-mode measurements: Ao=arotic root; LA=left atrium; IVS=ventricular septum; LVPW=left ventricular posterior wall; LVDd=left ventricular dimension in diastole; LVDs=left ventricular dimension in systole.
Results Subject characteristics Table 1 presents the general characteristics of the subjects studied. The sedentary controls were significantly older than the orienteers, but there were no differences in height, body mass or body surface area. The heart rate was significantly lower in the female orienteers compared with the sedentary controls.
Two-dimensional and M-mode measurements Echocardiographic data from the right and left cavity and wall measurements are shown in Tables 2–5. The Eur Heart J, Vol. 20, issue 4, February 1999
absolute measurements and measurements related to body surface area of the left and right cavity and wall dimensions are given. Reasons for excluding certain cross-sections from further analysis include poor technical imaging quality or when the region of interest exceeded the limit of the sector scan. The frequency in which measurements were possible is shown.
Left ventricular measurements The absolute left ventricular measurements and measurements related to body surface area are presented in Tables 2 and 3. The left ventricular wall was significantly larger in the athletes, the inter-ventricular septum
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Table 3 Two-dimensional and M-mode echocardiography: left ventricular and left atrial dimensions in 42 female elite orienteers and 32 sedentary female controls. Measurements related to body surface area (mm . m 1) Female orienteers
M-mode measurements Ao LA IVS LVPW LVDd LVDs 2-dimensional measurements Left ventricular chamber LV b LV 1 Left ventricular outflow tract LVOT Left ventricular inflow tract LVIT 3 Left atrium LA 1 LA b
Sedentary female controls
MV95% CI*
SD
n
MV95% CI*
SD
n
15·40·4 21·20·5 6·10·2 5·60·2 29·40·5 18·60·5
1·3 1·4 0·8 0·6 1·7 1·8
34 34 42 42 42 42
15·20·6 20·30·7 4·90·2 4·40·1 27·60·8 16·90·7
1·6 1·9 0·5 0·4 2·1 2·1
29 28 32 32 32 32
21·90·6 51·31·2
1·9 3·8
39 40
19·70·6 47·91·2
1·5 3·1
30 30
12·80·2
0·8
42
12·10·4
1·1
32
26·00·7
2·1
40
23·90·7
1·9
30
29·20·9 23·40·7
2·3 2·1
37 37
27·20·9 21·30·5
2·3 1·4
29 29
*Mean value and 95% confidence limits of the mean. Two-dimensional measurements; see text Fig. 1 for measurements and abbreviations. M-mode measurements: Ao=aortic root; LA=left atrium; IVS=ventricular septum; LVPW=left ventricular posterior wall; LVDd=left ventricular dimension in diastole; LVDs=left ventricular dimension in systole.
and the posterior wall were on average 17% and 19% larger, respectively, in the orienteers compared with the sedentary controls. Not one of the female athletes had left ventricular wall thickness >12 mm and only four athletes had left ventricular wall thickness >11 mm. The left ventricular cavity measurements were all slightly larger in the athletes, and the left ventricular enddiastolic cavity dimension was significantly (6%) greater in the athletes compared with the sedentary controls. No one had a left ventricular end-diastolic diameter exceeding 56 mm. Left atrial dimensions were not significantly larger in the athletes compared with the controls.
Right ventricular measurements The absolute right ventricular measurements and measurements related to body surface area are summarized in Tables 4 and 5. There were no significant differences in right ventricular cavity length, the -OT measurements or in the measurement in middle third of the right ventricular cavity, but all right ventricular -IT measurements were significantly larger (RVIT 1–3 10%, 13%, 12%) in the orienteers. The right ventricular free wall were measured at three sites. T1 and T5 were significantly larger, 14% and 16% respectively, in the athletes compared with the sedentary controls. Although T3 was slightly larger in the athletes (9%) this difference failed to reach statistical significance. The right ventricular wall thickness
calculated as the mean of the three wall measurements was significantly greater(13%) in the athletes compared with the sedentary controls.
Discussion The most important and probable reason for the lack of interest of the right ventricle among echocardiographers is the complex geometry of the right ventricle making imaging, accurate measurements and functional assessment difficult. Despite these difficulties, by using anatomical landmarks to standardize the orientation of the ultrasound beam within the right ventricle, measurements of the right ventricular cavity can be obtained[10]. Both the pulmonary and the systemic circulation must show a performance change to meet the circulatory demands of extensive and prolonged physical exercise. In addition these circulation systems must increase their cardiac output by the same amount during exercise. Except for the increase in heart rate, this can be attained by either increasing the end-diastolic volume or decreasing the end-systolic volume or both. The mechanisms by which the pulmonary circulation increases its cardiac output during exercise remains controversial. Morrison et al.[11] found that the right ventricular ejection fraction increased more than the left ventricular ejection fraction during supine exercise, which indicates a decrease in right ventricular end-diastolic volume during exercise. On the other hand Douglas et al.[12] found by means of Eur Heart J, Vol. 20, issue 4, February 1999
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Table 4 Two-dimensional echocardiography; right ventricular and right atrial dimensions in 42 female elite orienteers and 32 sedentary female controls. (Absolute measurements in mm) Female orienteers
Right ventricular chamber RV b RV 1 Right ventricular outflow tract RVOT 1 RVOT 3 RVOT 4 Right ventricular inflow tract RVIT 1 RVIT 2 RVIT 3 Tricuspid valve annulus RVA 1 Right ventricular wall thickness T1 T3 T5 Right atrium RA 1 RA b
Sedentary female controls
MV95% CI*
SD
n
MV95% CI*
SD
n
21·51·0 76·12·2
2·9 6·8
33 39
21·61·2 74·31·9
2·7 4·7
24 28
28·51·0 27·21·0 29·41·1
2·9 2·9 3·3
39 33 37
28·10·9 26·81·2 28·91·1
2·4 2·9 2·8
32 27 30
55·62·1 35·61·2 35·70·9
5·7 3·1 2·8
31 30 39
50·51·3 31·10·8 31·51·0
3·2 2·0 2·5
26 27 30
38·60·8
2·2
31
36·10·9
2·4
28
3·70·2 3·70·2 3·90·2
0·5 0·7 0·5
38 31 37
3·20·2 3·40·2 3·30·2
0·5 0·5 0·5
31 25 28
46·71·7 39·51·2
5·0 3·6
38 38
43·81·4 36·31·2
3·5 3·1
29 29
*Mean value and 95% confidence limits of the mean. Two-dimensional measurements; see text and Fig. 1 for measurements and abbreviations.
echocardiography that triathletes, after cessation of extreme exercise, had an increase in right ventricular end-diastolic cavity area and a decrease in left ventricular end-diastolic cavity area. Even if there is uncertainty about the right ventricular end-diastolic volume during exercise, investigators have shown important differences in workload between the right and the left ventricle during exercise. During exercise, the pulmonary vascular resistance is reduced less than the systemic resistance and the relative increase in pulmonary artery pressure is greater than the increase in the systemic arterial pressure[13–17], suggesting that the relative increase in cardiac load imposed on the right ventricle is greater than that in the left ventricle. Because the total cardiac work performed which is responsible for the structural changes, is described as ‘the athlete’s heart’, right ventricular adaptation to intense and prolonged physical exercise may be expected to increase the right ventricular cavity dimensions, with a concomitant increase in right ventricular contractile reserve. The present study supports this reasoning and shows that at rest the right ventricular inflow tract was significantly larger in female orienteers compared with the sedentary females. The right ventricular outflow tract and cavity length were similar between the study groups. However, right ventricular wall thickness, calculated as the mean of the three wall measurements, showed a significantly (13%) greater wall thickness in athletes compared with the sedentary controls. This suggests an ability of the right Eur Heart J, Vol. 20, issue 4, February 1999
ventricle to increase its contractile reserve to meet the circulatory demands of extensive and prolonged physical exercise. Distinguishing between physiological hypertrophy due to training and hypertrophy due to cardiac disease is a difficult but an important issue in sports medicine because hypertrophic cardiomyopathy is a common cause of sudden unexpected death in young athletes[18–20]. To make this distinction, which largely depends on whether the wall thickness exceeds that expected as a result of training, it is important to have knowledge about the upper physiological limits that result from training. These limits may be influenced by several factors, such as gender, level or intensity of athletic training, type of sport performed and genetic or racial background[22]. Previous studies have shown that the upper physiological limit for left ventricular wall thickness is in the range of 15–16 mm in male and c12 mm in female endurance athletes[1,6]. In this study, despite the thicker left ventricular wall in the female athletes, no athlete reached the morphological grey zone resembling hypertrophic cardiomyopathy.
Study limitations If the measurements in this paper are used as reference values they can only be extended to females of the ages cited in Table 1.
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Table 5 Two-dimensional echocardiography; right ventricular and right atrial dimensions in 42 female elite orienteers and 32 sedentary female controls. Measurements related to body surface area (mm . m 2) Female orienteers
Right ventricular chamber RV b RV 1 Right ventricular outflow tract RVOT 1 RVOT 3 RVOT 4 Right ventricular inflow tract RVIT 1 RVIT 2 RVIT 3 Tricuspid valve annulus RVA 1 Right ventricular wall thickness T1 T3 T5 Right atrium RA 1 RA b
Sedentary female controls
MV95% CI*
SD
n
MV95% CI*
SD
n
13·20·7 46·31·4
1·9 4·3
33 39
12·70·6 44·41·3
1·5 3·3
24 28
17·30·6 16·50·6 17·80·7
1·8 1·8 2·0
39 33 37
16·70·7 15·80·8 17·20·6
1·9 1·9 1·6
32 27 30
33·81·4 21·70·8 21·60·6
3·9 2·2 1·7
31 30 38
29·91·0 18·60·6 18·70·8
2·4 1·5 2·0
26 27 30
23·50·7
1·9
31
21·40·8
2·0
28
2·20·1 2·30·1 2·30·1
0·3 0·4 0·4
38 31 37
1·90·1 2·00·1 2·00·1
0·3 0·4 0·3
31 25 28
28·41·0 24·00·8
3·1 2·3
38 38
25·70·8 21·40·6
2·0 1·7
29 29
*Mean value and 95% confidence limits of the mean. Two-dimensional measurements; see text and Fig. 1 for measurements and abbreviations.
Conclusion This study suggest that symmetrical cardiac enlargement occurs in elite female orienteers, with a concomitant increase in both the right and left ventricular wall, probably reflecting the increased haemodynamic loading. The authors wish to express their appreciation to Mari-Louise Engstro¨m Walker for her assistance. These investigations were supported by funds from the Swedish Orienteering Federation, the Swedish Centre for Research in Sports, Bert von Kantow’s, A r ke Wiberg’s Foundation and a special grant from the Swedish Government.
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