and Cystic Fibrosis Centre, Rigshospitalet, Copenhagen, Denmark, 4Department of Clinical Physiology and Nuclear Medicine,. Frederiksberg Hospital ...
Scand J Med Sci Sports 2008: 18: 354–359 Printed in Singapore . All rights reserved DOI: 10.1111/j.1600-0838.2007.00706.x
Copyright & 2007 The Authors Journal compilation & 2007 Blackwell Munksgaard
Effect of eight weeks of endurance exercise training on right and left ventricular volume and mass in untrained obese subjects: a longitudinal MRI study T. W. Vogelsang1,2, B. Hanel3, U. S. Kristoffersen1,2, C. L. Petersen4, J. Mehlsen4, N. Holmquist5, B. Larsson6, A. Kjaer1,2 1
Cluster for Molecular Imaging, Department of Biomedicine, the Panum Institute, University of Copenhagen, Copenhagen, Denmark, Department of Clinical Physiology, Nuclear Medicine & PET, Rigshospitalet, Copenhagen, Denmark, 3Pediatric Pulmonary Service and Cystic Fibrosis Centre, Rigshospitalet, Copenhagen, Denmark, 4Department of Clinical Physiology and Nuclear Medicine, Frederiksberg Hospital, Copenhagen, Denmark, 5Centre for Higher Education, Ankerhus College of Nutrition and Health, Sorø, Denmark, 6Team Denmark Test Centre, Bispebjerg Hospital, Copenhagen, Denmark 2
Corresponding author: Thomas Wiis Vogelsang, M.Sc., Cluster for Molecular Imaging, Department of Biomedicine, the Panum Institute, University of Copenhagen, Denmark, Blegdamsvej 3, DK-2200 Copenhagen N, Denmark. Tel: (145) 35 32 75 33, Fax: (145) 35 32 75 55, E-mail: tvogelsang@mfi.ku.dk Accepted for publication 11 May 2007
The aim of the present investigation was to examine how 8 weeks of intense endurance training influenced right and left ventricular volumes and mass in obese untrained subjects. Ten overweight subjects (19–47 years; body mass index of 34 5 kg/m2) underwent intensive endurance training (rowing) three times 30 min/week for 8 weeks at a relative intensity of 72 8% of their maximal heart rate response (mean SD). Before and after 8 weeks of endurance training, the left and the right end-diastolic volume (EDV), end-systolic volume (ESV), ejection fraction (EF), stroke volume (SV) and ventricular mass (VM) were measured by Magnetic resonance imaging (MRI). Submaximal heart rate decreased from 126 5 to 113 3 b.p.m. (10%; Po0.01), and from 155 5 to 141 4 b.p.m. (9%;
Po0.001) at submaximal workloads of 70 and 140 W (110 W for women), respectively (mean SEM). Resting ventricular parameters increased significantly: left ventricular SV, EDV and VM increased by 6%, 7% and 13%, respectively (Po0.01). The right side of the heart showed significant changes in SV, EDV and VM with increase of 4%, 4% and 12%, respectively (Po0.05). Eight weeks of endurance training significantly increased left ventricular SV and right ventricular SV, due to an increase in left ventricular EDV and right ventricular EDV. Furthermore, left VM and right VM increased. We conclude that using MRI and a longitudinal design it was possible to demonstrate similar and balanced changes in the right and left ventricle in response to training.
Exercise training exerts numerous effects on the function and the morphology of the human heart. These adaptations are largely related to the type of exercise (Fagard et al., 1984; Mitchell et al., 1994). Strength training increases peripheral resistance, or afterload, and thereby leads to concentric hypertrophy, while endurance training increases venous return and blood volume, or preload, which stimulates an eccentric type of hypertrophy (Morganroth et al., 1975; Fleck, 1988; Becker, 1998). In some types of sport, e.g. rowing, there is both a strength and an endurance component involving dynamic and static exercise with large muscle groups (Pluim et al., 2000; Fagard, 2003). In the initial phase of the rowing stroke, the oarsmen perform a Valsalva-like manoeuvre, producing a large pulse pressure fluctuation superimposed on the normal pulse pressure, which may explain the greater cardiac hypertrophy in rowers (Clifford et al., 1994), compared with other endurance athletes.
Several methods are available for detection of the cardiac adaptations to exercise training, such as echocardiography (Pluim et al., 2000; Fagard, 2003), radionuclide angiography (Goodman et al., 2005) and magnetic resonance imaging (MRI) (Milliken et al., 1988; Doherty et al., 1992; Pluim et al., 1996; Scharhag et al., 2002), with MRI considered the gold standard for evaluation of cardiac morphology and function (Higgins & Sakuma, 1996). Most previous studies have focused on the changes in the left ventricle, while only a few have evaluated the right ventricle (Doherty et al., 1992; Scharhag et al., 2002). MRI is now a well-validated method also for analyzing the right side of the heart (Kjaer et al., 2005a). MRI has been used in the comparison of athletes and untrained (Scharhag et al., 2002). In the analysis of athletes’ hearts, most of the previous studies have been cross-sectional only (Pelliccia et al., 1991; Urhausen et al., 1996b; Urhausen et al., 1997; Urhausen & Kindermann, 1999). These studies used
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Exercise induced cardiac changes echocardiography to measure the difference in cardiac dimensions. Echocardiography measures have a much higher variability, making them less suited for detection of small changes in cardiac dimensions and/or studies in small groups. One study, using radionuclide angiography, examined the effect of training longitudinally on the left ventricle in a 6 day endurance-training regime. No significant changes in end-diastolic volume (EDV) , end-systolic volume (ESV) or stroke volume (SV) were found in that study (Goodman et al., 2005). MRI has, to our knowledge, never been used in evaluation of right- and-left sided cardiac morphology and mass in an interventional longitudinal exercise training study. Using MRI in a longitudinal protocol should allow for detection of even small changes in cardiac morphology and function. Therefore, the aim of the present investigation was to compare the morphology of the heart examined by MRI before and after eight weeks of endurance training. Rowing was used as training regime, due to the influence on both pre- and afterload. Eight weeks of training was chosen as a relatively short period of training where we could expect changes (Ray et al., 1990). It was possible to follow and intensively encourage the test persons for 8 weeks to obtain high compliance. This could probably not have been obtained if the period had been much longer. Furthermore, we hypothesized that 8 weeks of rowing training would induce morphological and structural changes in both the left and right ventricle in overweight untrained human subjects. The reason for using overweight subjects was that they represented a group that was reliably sedentary from the beginning and they were not expected to train if not included in this interventional study. Furthermore, they were highly motivated for intervention in the form of training. Finally, from a health prevention point of view, the subjects represent a highly relevant group, because they are at a high risk of developing obesity- and sedentary life style-related diseases and thereby they would also be a polulation that would benefit highly from exercise.
102 4 kg (74–113) and BMI 34.1 1.6 kg/m2 (25–40). Subjects were weighted before the bicycle test (Tanita WB 100MA, Tanita, France), wearing their sports clothes. They were not in a fasted state, but received the information to follow the same procedure at the days of testing. Resting heart rate was measured in the supine position during the MR scans. Preand post-training values of peak oxygen uptake (VO2peak) were determined from a progressive bicycle ergometer test to fatigue before and after the training period. Subjects were not engaged in any other regularly physical activity before and during the study period. Further, subjects had no restriction in their food intake during the study period, and none of the subjects were on any medication before or during the study period.
Methods
Assessment of cardiac function by MRI
Subjects Ten untrained (VO2peak: 23.0 5.3 mL O2/min/kg) and overweight subjects (seven women and three men) participated in the study. The subjects were recruited though the local newspaper. The inclusion criteria were that the subjects had to be untrained, not active in organized physical activity and having a body mass index (BMI) above 25 kg/m2. Exclusion criteria were known cardiovascular disease, diabetes or pregnancy. Written consent was obtained from all subjects before inclusion. The study was approved by the Ethics Committee of Copenhagen and Frederiksberg communities (KF 01-077/04). The physical characteristics for the subjects in the pre-training state were as follows: age of 32 8.9 years (18–46), weight
Bicycle ergometer test The subjects started cycling (Ergoselect 100, Ergoline, Germany) at 70 W for 5 min and then increased to 110 W for women and 140 W for men for another 5 min. Following these 10 min, the workload increased 20 W every minute until exhaustion. Peak oxygen uptake, VO2peak, was measured continuously during the test (OXYCON Pro, Jaeger, Kempele, The Netherlands) and the average of the three highest values was determined as the peak value. Heart rate was monitored at the end of every step by a heart rate monitor and a maximal value was monitored at exhaustion (Polar 625i, Polar Electro, Finland). The bicycle ergometer test for testing the cardiovascular improvements was used because the subjects were unfamiliar with the rowing technique at the beginning of the study period. Using a rowing ergometer test at the beginning of the study, we would not have obtained reliable results.
Training procedure The subjects were training in a rowing ergometer (Concept II, Morrisville, Vermont, USA). After giving instructions three times on how to use the rowing ergometer, subjects trained 30 min three times per week for 8 weeks with a relative intensity of 75% of their maximal heart rate response. The relative intensity was calculated as an average over the active intervals; the actual time spent at the relative intensity of 75% was 20–25 min. Each training session consisted of intervals of various lengths (5–25 min) with breaks of 2–5 min. Warm-up was included in the 30-min session. Because of injuries, three of the subjects had to replace the rowing ergometer with a cycle ergometer for a few training sessions. All training sessions were supervised by one of the authors. Further, training sessions were heart rate controlled (Polar 625i, Polar Electro) to ensure that the training intensity was maintained.
MRI is a volumetric technique based on visualization of the anatomy of the ventricle, which does not require injection of a contrast agent. The technique gives precise anatomical information. MRI was performed on a 1.5-T whole-body scanner (Intera, Philips, Best, The Netherlands) using a dedicated phased array cardiac coil (Synergy, Philips). Following localization of the long axis of the heart, contiguous true short-axis slices were acquired using breath hold, ECG-triggered cine MRI. Slices were obtained during one breath hold of 6–10 s. Typically, the heart was covered by 10–15 slices of 10 mm. The number of phases obtained was 30. The field of view was 320 mm with a matrix of 256 256. A turbo field echo (B-TFE) M2D cine MRI with breath-hold was used (Intera, Philips,
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Vogelsang et al. release 10.3). The sequence parameters were relaxation time TR 5 3.2 ms, echo time TE 5 1.6 ms and flip angle FA 5 601. The endocardial contours of the left and right ventricle were traced manually on all phases and slices using standard software (Philips ViewForum release 3.2). On the most basal slice, the right atrium and the pulmonary artery were avoided. The analysis started in all cases by viewing the slice dynamically in movie-mode to gain an overall impression of movements, including shortening and to visualize the functional separation of right ventricle and atrium. Following this, the endocardial contour was drawn on all phases. The end-systole and enddiastole frames were defined as the phases with the highest and lowest volume, respectively. In practice, this led to phase one always being end-diastole. The right ventricle end-systole was not always the same as the end-systole of the left ventricle but could be one phase apart. RV-EDV and ESV and RV-EF were then automatically calculated adding the volumes of each slice. Epicardial contours were traced manually and the end-diastolic frame and the mass calculated as myocardial volume multiplied by a density 1.05 g/mL. The studies were read by two independent observers in a blinded manner at the end of the study in a mixed order. In the case of discrepancy, consensus was obtained by the readers. The inter-observer variability between the two examiners in the present study has been established previously in our laboratory. Expressed as SD on the difference (SDD) the inter-observer variability was: LV-EF: 0.03 (4.6%); LV-SV: 4.9 mL (5.9%); LV-EDV: 6.0 mL (5.5%); LV-ESV: 4.5 mL (15.3%); LVM: 7.3 g (4.2%); RV-EF: 0.04 (6.5%); RV-SV; 5.2 mL (6.7%); RV-EDV: 6.0 mL (4.8%); RV-ESV: 6.4 mL (14.0%); and RVM: 5.0 g (10.3%).
Statistical analysis Data are presented as mean SEM (or range). Values before and after eight weeks of endurance training were compared by a one-sided paired t-test. We used a one-sided model, because we anticipated a priori that the data would evolve in a certain direction. In case of regression, we used a linear model. Po0.05 was considered to be significant. SPSS v. 13.0 (SPSS Inc., Chicago, Illinois, USA) was used for analysis.
Results Subject characteristics Eight weeks of rowing training did not change the body weight, BMI or body surface area (BSA) (Table 1).
Cardiovascular changes Eight weeks of rowing training increased the peak oxygen consumption (VO2peak), with 15% from a baseline value of 23.0 2.0 mL O2/min/kg to 26.5 2.7 mL O2/min/kg (Po0.02). Heart rate at submaximal workloads decreased significantly from 126.0 5 to 113 3 b.p.m. (Po0.01) and from 155 5 to 141 4 (Po0.001) at 70 and 140 W (110 W for women), respectively. Time to exhaustion increased from 15.3 1.0 min to 17.1 0.9 min before and after the training period, respectively (Po0.01). Maximal heart rate was 182 4 and 178 3 bpm before and after the training period, respectively (NS). Data are summarized in Table 1. Ventricular mass (VM) The LV and RV masses are presented in Fig. 1. Following 8 weeks of rowing training, the LV mass increased by 13% from 162.3 9.5 to 183.2 12.6 g (Po0.01) and the RV mass increased 12% from 42.6 3.3 to 47.7 3.9 g (Po0.05). The indexed masses (values divided by BSA) showed a similar increase of 13% and 12% for LV (Po0.01) and RV (Po0.05), respectively. The ratio of LV to RV mass was unchanged by exercise training (Fig. 1). LV mass correlated significantly with VO2peak, both before and after the training period (r 5 0.65; Po0.05 and r 5 0.67; Po0.05, respectively). Ventricular volume LV-EDV was significantly increased by 7% from 153.1 10.4 to 163.3 10.7 mL in the training period (Po0.01). At the right side of the heart, RV-EDV increased 4% from 177.7 13.7 to 184.0 15.4 mL (Po0.05; Fig. 2). Indexed LVEDV and RV-EDV values showed similar differences, although changes in RV-EDV did not reach significance (P 5 0.054).
Table 1. Effect of 8 weeks of rowing training
Weight, (kg) BMI, (kg/m2) BSA, (m2) Resting heart rate, (beats/min) Maximal heart rate (beats/min) Sub-maximal heart rate, (beats/min) 70 W 110/140 W VO2peak, (mL/min/kg) Time to exhaustion (min)
Pre-training
Post-training
P value
102.2 3.7 34.1 1.6 2.6 0.1 68.3 2.5 182 4
101.7 4.4 33.9 1.7 2.6 0.1 65.9 2.8 178 3
NS NS NS NS NS
126 5 155 5 23.0 1.7 15.3 1.0
113 3 141 4 26.5 2.7 17.1 0.9
0.01 0.01 0.02 0.01
Pre- and post-training values of weight, resting heart rate, sub-maximal heart rate at the two different workloads, peak oxygen consumption (VO2peak), and P values. Values are mean SEM. BMI, body mass index; BSA, body surface area.
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Exercise induced cardiac changes **
5 4
150
3 100
** 2
*
50
* 0
LV
RV
LV Index RV Index LV / RV
Ratio (LV / RV)
Myocardial Mass (g) Myocardial Mass Index (g/m2)
200
1 0
2
250
*
200 150
1 100
*
50 0
LV
RV
LV Index RV Index LV / RV
0
Fig. 2. End-diastolic volume, end-diastolic volume index (end-diastolic volume divided by body surface area), and ratio of left ventricular (LV) to right ventricular (RV) enddiastolic volume before (black bars) and after 8 weeks of endurance exercise training (white bars). Data are presented as mean SEM. *Po0.05 compared with the untrained state; **Po0.01 compared with the untrained state.
140
2
**
*
100 80 1 60 40
Ratio (LV / RV)
Stroke Volume (ml) Ejection Fraction (%)
120
20 0
Ventricular function SV, ejection fractions (EFs) and ratios are presented in Fig. 3. Training increased LV-SV significantly by 6% from 105.2 7.5 to 111.3 7.6 mL (Po0.01), and RV-SV by 4% from 105.1 7.6 to 109.2 8.1 mL (Po0.05). The indexed SV data showed similar differences, although RV-SVI did not reach significance (P 5 0.056). Neither LV-EF nor RV-EF showed any differences between the untrained and trained state. The LV-SV to RV-SV ratio, as well as the LV-EF to RV-EF ratio did not show any difference during the training period. Finally, no difference was observed in resting cardiac index (3.2 0.2 vs 3.3 0.2 mL/min/kg2) in response to exercise training. Discussion
**
Ratio (LV / RV)
End-Diastolic Volume (ml) End-Diastolic Volume Index (ml/m2)
Fig. 1. Myocardial mass, myocardial mass index (myocardial mass divided by body surface area) and ratio of left ventricular (LV) to right ventricular (RV) mass in the untrained state (black bars) and after 8 weeks of endurance exercise training (white bars). Data are presented as mean SEM. *Po0.05 compared with the untrained state; **Po0.01 compared with the untrained state.
The LV-EDV to RV-EDV ratio did not differ in the pre- and post-training conditions. No significant changes were observed in either the LV-ESV and RV-ESV or the indexed ESV values.
LV-SV RV-SV LVEF
RVEF SV ratio EF ratio
0
Fig. 3. Stroke volume, ejection fraction (EF), ratio of left ventricular (LV) and right ventricular (RV) stroke volume (SV ratio), and ratio of LVEF to RVEF (EF ratio) before (black bars) and after eight weeks of endurance exercise training (white bars). Data are expressed as mean SEM. *Po0.05 compared to the untrained state; **Po0.01 compared with the untrained state.
The present study, using the MRI technique, evaluated the longitudinal effect on heart morphology during 8 weeks of endurance training in untrained overweight subjects. We found significant morphological changes in the right and left ventricle after this relatively short period of endurance training. In the untrained state, the subject had an average LV mass of 163 g and 75 g/m2 when normalized to BSA (LVMI), which is in accordance with previously reported mean values for healthy subjects of 107– 189 g and LVMI of 69–96 g/m2, respectively (Doherty et al., 1992; Pluim et al., 1998; Lorenz et al., 1999). The increase of mean LV mass to 183 g and LVMI to 85 g/m2 after 8 weeks of rowing training is still within the previously reported mean values. Using normalized values, the VM indexes in our subjects were in the middle of the previously reported mean values due to the large BSA. At the right side of the heart, the mean RV mass increased from 43 g and RVMI of 20 g/m2–48 g and 22 g/m2 after the training period. In agreement with other MRI studies, the mean values for RV mass have been reported to range from 37 to 56 g (Doherty et al., 1992; Katz et al., 1993; Pattynama et al., 1995; Lorenz et al., 1999; Scharhag et al., 2002). Previous studies have indexed the RV mass to BSA in and found mean values in the range of 23–30 g/m2 in healthy control subjects (Katz et al., 1993; Lorenz et al., 1999; Scharhag et al., 2002). In the present investigation, both the pre- and post-training mean values of indexed RV mass were slightly lower than the previously reported mean values. This could probably be explained by a larger BSA in our study population compared with previous studies (Katz et al., 1993; Scharhag et al., 2002).
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Vogelsang et al. The magnitudes of LV-EDV were similar to those reported in previous MRI studies (Sechtem et al., 1987; Milliken et al., 1988; Buser et al., 1989; Semelka et al., 1990; Pattynama et al., 1995; Pluim et al., 1998; Lorenz et al., 1999) . RV-EDV data were also within the range of earlier reported values (Doherty et al., 1992; Scharhag et al., 2002). Both left and right ventricular EDV increased significantly during endurance training, and the observed increase in both right- and left-sided SV could be explained by the Frank–Starling mechanism. The increments in cardiac mass were most likely related to the changes in chamber size, as this, by the law of LaPlace, would elevate wall stress, and trigger a positive feedback loop stimulating an eccentric hypertrophic response in an attempt to normalize the elevated wall stress (Hood et al., 1968; Grossman et al., 1975). It should be noted that even after training, our subjects did not have hypertrophy as defined as mass above normal limits. In accordance with a previous study comparing athletes’ hearts and those of sedentary control subjects, we did not observed any difference in the LVEDV to RV-EDV ratio before and after exercise training, which may indicate a balanced biventricular myocardial hypertrophy and a balanced biventricular dilation (Scharhag et al., 2002). It has been stated that it takes more than 3 h of exercise per week to change left VM(Fagard, 2003). The present investigation showed significant changes in the left VM, using a rowing training program for 30 min three times per week for 8 weeks. This discrepancy may be due to an improvement in the sensitivity of the imaging methods. We used MRI to detect differences caused by endurance training, whereas others have used echocardiography (Morganroth et al., 1975; Urhausen et al., 1996a; Fagard, 1997; Pluim et al., 2000; Hoogsteen et al., 2004) or radionuclide angiography (Goodman et al., 2005). The advantage of the MRI technique is its low variability and high reproducibility allowing for detection of smaller changes than other imaging modalities. Furthermore, we used a paired design studying the same subjects before and after training, also allowing for detection of smaller differences. A possible reason for the increase in cardiac dimensions could be an increase in plasma volume. In the present investigation we did not measure any hematological variables to prove this hypothesis; however, it has been shown previously that an increase in plasma volume may be about 5% (Schmidt et al., 1988). This exercise-induced increase in plasma volume would correspond very well with the increase in EDV found in the present study. The data obtained during exercise showed an increase in VO2peak and a decrease in heart rate during a two-stage submaximal bicycle ergometer
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test, which indicated an improvement in the cardiovascular function. It is slightly surprising that the resting heart rate did not significantly change in response to the training. However, the average did indeed decrease but this did not reach significance probably due to a statistical type II error caused by the limited number of subjects. However, we cannot totally rule out that to some extent habituation to the exercise test contributed to the observed changes in heart rate during exercise. In summary, 8 weeks of rowing training in obese subjects led to a significant increase in SV, due to an increase in EDV and VM in both the right and left side of the heart. We conclude that using MRI and a longitudinal design, it was possible to demonstrate a similar and balanced change in the right and left ventricle in response to training, even after a relatively short training period.
Perspectives Our findings of changes in cardiac function and morphology in sedentary, obese subjects after only 8 weeks of training are encouraging. They demonstrate that training makes a difference even when the daily amount is moderate. If we believe that the training-induced changes are beneficial, e.g. traning-induced ventricular hypertrophy (Kjaer et al., 2005b), both with respect to capacity and thereby quality of life and also in order to prevent cardiovascular disease, we have shown that in a group at risk, obese subjects, effects may be obtained with rather small ‘‘sacrifices.’’ The results could be used as a motivator to get sedentary subjects started with exercise. The present study also demonstrates the value of using high-precision methods to be able to demonstrate moderate changes in small populations. It has been shown previously that cardiac MRI compared with e.g. echocardiography allows for a often more than 10-fold reduction in sample size (Bellenger et al., 2000). Accordingly, the use of cardiac MRI seems to be a powerful tool for the study of traininginduced changes of the heart. Key words: magnetic resonance imaging, ventricular hypertrophy, exercise training, athlete’s heart, rowing.
Acknowledgement We thank Elsa Larsen and Michael Westfeldt Johansen for skilled technical assistance. This study was supported by the Danish Medical Research Council, The Læge Sophus Carl Emil Friis og hustru Olga Doris Friis Foundation, The A. P. Møller Foundation for the Advancement of Medical Science & Konsul Ehrenfried Owese´n og Hustrus Foundation.
Exercise induced cardiac changes References Becker AE. Myocardial remodeling and its complications. In: Willis Hurst J., ed. Atlas of the heart. New York: McGraw-Hill, 1998: 21–27. Bellenger NG, Davies LC, Francis JM, Coats AJ, Pennell DJ. Reduction in sample size for studies of remodeling in heart failure by the use of cardiovascular magnetic resonance. J Cardiovasc Magn Reson 2000: 2: 271–278. Buser PT, Auffermann W, Holt WW, Wagner S, Kircher B, Wolfe C, Higgins CB. Noninvasive evaluation of global left ventricular function with use of cine nuclear magnetic resonance. J Am Coll Cardiol 1989: 13: 1294–1300. Clifford PS, Hanel B, Secher NH. Arterial blood pressure response to rowing. Med Sci Sports Exerc 1994: 26: 715–719. Doherty NE III, Fujita N, Caputo GR, Higgins CB. Measurement of right ventricular mass in normal and dilated cardiomyopathic ventricles using cine magnetic resonance imaging. Am J Cardiol 1992: 69: 1223–1228. Fagard R, Aubert A, Staessen J, Eynde EV, Vanhees L, Amery A. Cardiac structure and function in cyclists and runners. Comparative echocardiographic study. Br Heart J 1984: 52: 124–129. Fagard RH. Impact of different sports and training on cardiac structure and function. Cardiol Clin 1997: 15: 397–412. Fagard RH. Athlete’s heart. Heart 2003: 89: 1455–1461. Fleck SJ. Cardiovascular adaptations to resistance training. Med Sci Sports Exerc 1988: 20: S146–S151. Goodman JM, Liu PP, Green HJ. Left ventricular adaptations following short-term endurance training. J Appl Physiol 2005: 98: 454–460. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 1975: 56: 56–64. Higgins CB, Sakuma H. Heart disease: functional evaluation with MR imaging. Radiology 1996: 199: 307–315. Hood WP Jr., Rackley CE, Rolett EL. Wall stress in the normal and hypertrophied human left ventricle. Am J Cardiol 1968: 22: 550–558. Hoogsteen J, Hoogeveen A, Schaffers H, Wijn PF, Van Hemel NM, van der Wall EE. Myocardial adaptation in different endurance sports: an echocardiographic study. Int J Cardiovasc Imaging 2004: 20: 19–26. Katz J, Whang J, Boxt LM, Barst RJ. Estimation of right ventricular mass in
normal subjects and in patients with primary pulmonary hypertension by nuclear magnetic resonance imaging. J Am Coll Cardiol 1993: 21: 1475–1481. Kjaer A, Lebech AM, Hesse B, Petersen CL. Right-sided cardiac function in healthy volunteers measured by firstpass radionuclide ventriculography and gated blood-pool SPECT: comparison with cine MRI. Clin Physiol Funct Imaging 2005a: 25: 344–349. Kjaer A, Meyer C, Wachtell K, Olsen MH, Ibsen H, Opie L, Holm S, Hesse B. Positron emission tomographic evaluation of regulation of myocardial perfusion in physiological (elite athletes) and pathological (systemic hypertension) left ventricular hypertrophy. Am J Cardiol 2005b: 96: 1692–1698. Lorenz CH, Walker ES, Morgan VL, Klein SS, Graham TP Jr. Normal human right and left ventricular mass, systolic function, and gender differences by cine magnetic resonance imaging. J Cardiovasc Magn Reson 1999: 1: 7–21. Milliken MC, Stray-Gundersen J, Peshock RM, Katz J, Mitchell JH. Left ventricular mass as determined by magnetic resonance imaging in male endurance athletes. Am J Cardiol 1988: 62: 301–305. Mitchell JH, Haskell WL, Raven PB. Classification of sports. Med Sci Sports Exerc 1994: 26: S242–S245. Morganroth J, Maron BJ, Henry WL, Epstein SE. Comparative left ventricular dimensions in trained athletes. Ann Intern Med 1975: 82: 521–524. Pattynama PM, Lamb HJ, Van d V, van der Geest RJ, van der Wall EE, de RA. Reproducibility of MRI-derived measurements of right ventricular volumes and myocardial mass. Magn Reson Imaging 1995: 13: 53–63. Pelliccia A, Maron BJ, Spataro A, Proschan MA, Spirito P. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med 1991: 324: 295–301. Pluim BM, Chin JC, De Roos A, Doorn bos J, Siebelink HM, Van der Laarse A, Vilegen HW, Lemerichs RM, Bruschke AV, Van der Wall EE. Cardiac anatomy, function and metabolism in elite cyclists assessed by magnetic resonance imaging and spectroscopy. Eur Heart J 1996: 17: 1271–1278. Pluim BM, Lamb HJ, Kayser HW, et al. Functional and metabolic evaluation of the athlete’s heart by magnetic
resonance imaging and dobutamine stress magnetic resonance spectroscopy. Circulation 1998: 97: 666–672. Pluim BM, Zwinderman AH, van der LA, van der Wall EE. The athlete’s heart. A meta-analysis of cardiac structure and function. Circulation 2000: 101: 336–344. Ray CA, Cureton KJ, Ouzts HG. Postural specificity of cardiovascular adaptations to exercise training. J Appl Physiol 1990: 69: 2202–2208. Scharhag J, Schneider G, Urhausen A, Rochette V, Kramann B, Kindermann W. Athlete’s heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging. J Am Coll Cardiol 2002: 40: 1856–1863. Schmidt W, Maassen N, Trost F, Boning D. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur J Appl Physiol Occup Physiol 1988: 57: 490–498. Sechtem U, Pflugfelder PW, Gould RG, Cassidy MM, Higgins CB. Measurement of right and left ventricular volumes in healthy individuals with cine MR imaging. Radiology 1987: 163: 697–702. Semelka RC, Tomei E, Wagner S, Mayo J, Kondo C, Suzuki J, Caputo GR, Higgins CB. Normal left ventricular dimensions. and function: interstudy reproducibility of measurements with cine MR imaging. Radiology 1990: 174: 763–768. Urhausen A, Kindermann W. Sportsspecific adaptations and differentiation of the athlete’s heart. Sports Med 1999: 28: 237–244. Urhausen A, Monz T, Kindermann W. Sports-specific adaptation of left ventricular muscle mass in athlete’s heart. I. An echocardiographic study with combined isometric and dynamic exercise trained athletes (male and female rowers). Int J Sports Med 1996a: 17(Suppl. 3): S145–S151. Urhausen A, Monz T, Kindermann W. Sports-specific adaptation of left ventricular muscle mass in athlete’s heart. II: an echocardiographic study with 400-m runners and soccer players. Int J Sports Med 1996b: 17(Suppl. 3): S152–S156. Urhausen A, Monz T, Kindermann W. Echocardiographic criteria of physiological left ventricular hypertrophy in combined strength- and endurance-trained athletes. Int J Card Imaging 1997: 13: 43–52.
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