Background
The term endurance sport (ES) is broadly used to characterize any exercise that requires maintenance of high cardiac output over extended time. However, the relative amount of isotonic (volume) versus isometric (pressure) cardiac stress varies across ES disciplines. To what degree ES-mediated cardiac remodeling varies, as a function of superimposed isometric stress, is uncertain. The aim of this study was to compare the cardiac remodeling characteristics associated with two common yet physiologically distinct forms of ES.
Methods
Healthy competitive male long-distance runners (high isotonic, low isometric stress; n = 40) and rowers (high isotonic, high isometric stress; n = 40) were comparatively studied after 3 months of sport-specific exercise training with conventional and speckle-tracking two-dimensional echocardiography.
Results
Rowers demonstrated dilated left ventricular (LV) volumes and elevated LV mass (i.e., eccentric LV hypertrophy), whereas runners demonstrated normal LV mass (runners, 88 ± 11 g/m 2 ; rowers, 108 ± 13 g/m 2 ; P < .001) despite comparatively larger LV volumes (runners, 101 ± 10 mL/m 2 ; rowers, 89 ± 13 mL/m 2 ; P < .001) consistent with eccentric LV remodeling. Increasing LV mass was associated with increased reliance on early diastolic filling (LV mass vs E′/A′ ratio, R = 0.47, P < .001) indicating “mass-dependent” diastolic function. Right ventricular dilation of similar magnitude and LV systolic function, as assessed by numerous complementary indices, were similar in both groups.
Conclusions
Cardiac adaptations differ significantly as a function of ES discipline. Further work is required to determine the mechanisms for this differential adaptation, to develop definitive ES discipline-specific normative values, and to evaluate the optimal therapeutic use of specific ES disciplines among patients with common cardiovascular diseases.
Highlights
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The degree of isometric cardiac stress varies across ES disciplines.
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Athletes practicing low (running) and high (rowing) isometric ES were studied with echocardiography after 3 months of intensive discipline-specific exercise training.
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Rowers demonstrated elevated LV mass and volume (eccentric LVH).
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Runners demonstrated normal LV mass despite larger LV volumes (eccentric LV remodeling).
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Increasing LV mass was associated with greater enhancement of early diastolic filling.
Routine vigorous physical exercise stimulates changes in cardiac structure and function. The process of exercise-induced cardiac remodeling (EICR) is driven largely by the increases in intracardiac pressure and volume that occur during moderate- to high-intensity exercise. Strength-based exercise involves short but repetitive bursts of intense skeletal muscle contraction (i.e., isometric physiology), which is accompanied by marked increases in system arterial pressure and relatively little augmentation in cardiac output. In contrast, endurance-based exercise is characterized by sustained rhythmic muscular activity (i.e., isotonic physiology) that requires substantial increases in cardiac output with variable amounts of arterial pressure rise. Prior cross-sectional data and longitudinal studies have demonstrated that endurance- and strength-based exercise lead to divergent forms of left ventricular (LV) EICR.
However, isometric and isotonic stresses represent two opposite ends of an exercise physiology spectrum and rarely occur in isolation as most athletic activities involve a combination of these two principal forms of hemodynamic stress. This is particularly true across the endurance sport (ES) disciplines, which all impart a high isotonic load on the cardiovascular system but vary considerably with respect to the degree of concomitant isometric physiology. Specifically, ES including rowing, cycling and triathlon involve a combination of high isotonic and high isometric stress while ES such as long distance running, orienteering, and soccer impart high isotonic but low isometric stress. Prior investigation has generally regarded all ES as equal with regards to the hemodynamic stress placed on the heart. To our knowledge, the degree to which EICR varies across ES disciplines as a function of the inherent amount of isometric stress has not been rigorously examined.
We therefore examined cardiac structure and function in competitive athletes who participate in two forms of ES characterized by widely different degrees of isometric physiology. We hypothesized that rowers (high isotonic, high isometric physiology) would demonstrate distinctly different cardiac parameters, specifically more pronounced LV hypertrophy (LVH), than long-distance runners (high isotonic, low isometric physiology). To address this hypothesis, we performed comprehensive echocardiographic characterization of competitive rowers and runners that were otherwise matched with respect to age, gender, and exercise capacity.
Methods
Study Design and Subjects
We used a retrospective, cross-sectional study design to compare cardiac structure and function among competitive collegiate rowers and long-distance runners. Participants were enrolled as part of the Harvard Athlete Initiative, a research program designed to study cardiovascular health and physiology in student athletes. We enrolled male athletes ≥18 years of age who were free of cardiovascular disease. Written informed consent was obtained from all participants. The Partners Human Research Committee and Harvard University institutional review board approved the protocol before initiation.
Participants were recruited varsity athletes who participated in sport-specific training as dictated by coaching staff members. Participants were studied at time points coinciding with peak or near peak fitness according to annual training cycles. All study measurements were made in the morning hours, and participants were required to have abstained from exercise training for ≥24 hours before assessment. Specifically, distance runners were studied at the immediate conclusion of the summer training season, which is used to prepare for the autumn season cross-country (10 km) races and is characterized by the highest annual training load. Rowers were studied at the immediate conclusion of autumn training season, a similarly high-volume training period used to prepare for spring season regattas. Subjects were excluded if they undertook any breaks of ≥3 days during the 3 months before study measurements.
Information including age, medication and/or supplement use, personal and family medical history, height, weight, and resting vital signs was obtained for each participant at the time of echocardiographic assessment. Participants were confidentially questioned regarding use of illicit performance-enhancing agents, subjected to drug testing according to National Collegiate Athletic Association recommendations, and excluded from participation if history of use was elicited. Training volume over the preceding 3 months was quantified as hours per week and was divided into endurance training (rowing, running, cycling, etc.) and strength training (weight lifting, plyometrics, etc.)
Echocardiography
Echocardiography was performed using a commercially available system (Vivid-I; GE Healthcare, Milwaukee, WI) with a 1.9- to 3.8-MHz phased-array transducer. Images were obtained after 20 min of rest and were separated from the previous training session by ≥12 hours. Two-dimensional and tissue Doppler imaging from standard parasternal and apical positions was performed by a single experienced sonographer. All data were stored digitally, and poststudy offline data analysis (EchoPAC version 7; GE Healthcare) was performed by one of two study cardiologists (M.M.W, R.B.W). Definitions of normality for cardiac structure and function were adopted from American Society of Echocardiography guidelines.
LV ejection fraction, LV end-diastolic volume (LVEDV), and LV end-systolic volume were calculated using the biplane modified Simpson technique. LV mass was calculated using the area-length method. Relative wall thickness was defined as [interventricular septal thickness (mm) + posterior wall thickness (mm)/LV internal end-diastolic diameter (mm)]. Right ventricular (RV) parameters were calculated as detailed by American Society of Echocardiography guidelines. All measurements were made as an average of three consecutive cardiac cycles. Measurements are presented both as raw data and adjusted for body surface area (BSA) when appropriate.
Comprehensive assessment of myocardial mechanics using speckle-tracking analysis and tissue Doppler was performed as previously reported by our group. Briefly, longitudinal tissue velocities (E′, A′, and S′) were measured from color-coded tissue Doppler images. Longitudinal strain was measured using speckle-tracking of an apical four-chamber view, and circumferential strain was assessed in the parasternal short-axis view at the mid papillary muscle level. Reported strain values reflect the average of the six myocardial segments that are prespecified by the analysis software. Individuals without complete six-segment data were excluded from analyses (longitudinal strain: n = 6 runners, n = 9 rowers; circumferential strain: n = 9 runners, n = 10 rowers). Twist mechanics were measured using short-axis images obtained at the basal and apical ventricular planes according to standardized criteria as previously described. Peak systolic apical rotation, basal rotation, LV twist, and peak diastolic untwisting rate were manually calculated using raw data.
Cardiopulmonary Exercise Testing
A randomly selected subgroup of runners ( n = 7) and rowers ( n = 11) were recruited to perform maximal, effort-limited cardiopulmonary exercise testing in conjunction with echocardiography. Participants abstained from exercise for >24 hours before testing. Participants performed incremental exercise using an upright cycle ergometer (CPE 2001; Medical Graphics, St. Paul, MN) equipped with an electronically braked ergometer (Warren Collins, Braintree, MA). A mouthpiece and nose clips were in place during exercise to facilitate measurements of gas exchange and ventilation. Pulmonary gas exchange and minute ventilation were measured breath by breath with a commercially available metabolic cart (CPX/D; Medical Graphics). The initial workload was 0 W/min and was increased by 25 W/min until volitional exhaustion. Subjects were considered to have reached their peak oxygen consumption (V o 2peak ) when the following criteria were met: (1) leveling off of oxygen consumption with increasing workload, (2) respiratory exchange ratio values > 1.1, and (3) heart rate of ≥90% of age-predicted maximum. V o 2peak was defined as the highest 15-sec average during the final minute of exercise.
Statistical Analysis
Measurements are presented as mean ± SD. Significance of differences between the two groups was assessed using two-tailed unpaired t tests or Wilcoxon rank sum tests as appropriate for the data distribution. Relationships between variables were assessed using the Spearman correlation coefficient. SPSS version 21.0 (IBM, Armonk, NY) and Prism 6.0 (GraphPad Software, San Diego, CA) were used for data analyses and graphical data representation. Two-tailed P values < .05 were considered to indicate statistical significance.
Results
Study Population
Characteristics of the two study groups are shown in Table 1 . The runner and rower cohorts each comprised 40 male Caucasian athletes (mean age: runners, 18.7 ± 0.8 years; rowers, 18.9 ± 0.4 years). Rowers were significantly taller and heavier than runners (mean BSA: rowers, 1.94 ± 0.1 m 2 ; runners, 1.81 ± 0.1 m 2 ; P < .001). The two groups had similar resting heart rates and blood pressures. Over the 3 months preceding the study time point, both groups performed similar volumes of sport-specific endurance-based exercise training (runners, 10.6 ± 3 h/wk; rowers, 10.9 ± 1 h/wk) and similar relatively low volumes of dedicated strength-based exercise training (runners, 1.5 ± 1 h/wk; rowers, 1.0 ± 1 h/wk). V o 2peak among the subgroup of participants who underwent cardiopulmonary exercise testing was similar (runners, 64 ± 9 mL/kg/min; rowers, 67 ± 8 mL/kg/min; P = NS).
| Variable | Runners ( n = 40) | Rowers ( n = 40) |
|---|---|---|
| Age (y) | 18.7 ± 0.8 | 18.9 ± 0.4 |
| Height (cm) | 179 ± 7 | 182 ± 5 † |
| Weight (kg) | 65.7 ± 6 | 74.2 ± 4 ‡ |
| BSA (m 2 ) | 1.81 ± 0.1 | 1.94 ± 0.1 ‡ |
| Heart rate (beats/min) | 58 ± 10 | 62 ± 9 |
| Systolic blood pressure (mm Hg) | 120 ± 11 | 117 ± 7 |
| Diastolic blood pressure (mm Hg) | 64 ± 6 | 59 ± 5 |
| Endurance training (h/wk) | 10.6 ± 2 | 10.9 ± 1 |
| Strength training (h/wk) | 1.5 ± 1 | 1.0 ± 1 |
| Peak oxygen consumption (mL/kg/min) ∗ | 64 ± 9 | 67 ± 8 |
∗ Data available on V o 2peak for seven runners and 11 rowers.
LV Structure
LV structural parameters are shown in Table 2 . Runners had larger LVEDVs than rowers (runners, 182 ± 21 mL; rowers, 172 ± 25 mL; P = .05), and this difference was further amplified after indexing for BSA (101 ± 10 vs 89 ± 13 mL/m 2 ; P < .001). The higher LVEDVs observed among runners were attributable both to comparatively larger LV internal diastolic dimensions (27.9 ± 2 vs 27.1 ± 2 mm/m 2 ; P < .001) and LV lengths (5.2 ± 0.4 vs 4.9 ± 0.4 cm/m 2 ; P < .05). Notably, 97% of runners (38 of 39) and 92% of rowers (37 of 40) demonstrated indexed LVEDV values in excess of normal values (LVEDV/BSA ≥ 75 mL) ( Figure 1 A) proposed for clinical use. In contrast, rowers demonstrated thicker LV walls (average wall thickness: rowers, 9.5 ± 1.0 mm; runners, 8.1 ± 0.8 mm) and greater absolute and BSA-indexed LV mass (108 ± 13 vs 88 ± 11 g/m 2 ; P < .001) than runners ( Table 2 ). No runner had an average wall thickness > 10.9 mm (the recommended upper limit of normal), while 10% of rowers (four of 40) exceeded this value ( Figure 1 B). Similarly, the vast majority of runners (36 of 40 [90%]) had LV mass values that fell within in the normal range (LV mass/BSA < 103 g/m 2 ), while the majority of rowers (24 of 38 [62%]) met LV mass criteria for hypertrophy ( Figure 1 C). Relative wall thickness, though statistically higher among rowers (0.37 ± 0.04 vs 0.32 ± 0.04, P < .001), was <0.43 in both endurance athlete cohorts, indicating eccentric LV geometry ( Figure 1 D).
| Variable | Runners ( n = 40) | Rowers ( n = 40) |
|---|---|---|
| LVIDd (mm) | 50.3 ± 3 | 52.4 ± 3 ‡ |
| LVIDd/BSA (mm/m 2 ) | 27.9 ± 2 | 27.1 ± 2 † |
| LVIDs (mm) | 34.4 ± 3 | 35.5 ± 2 ∗ |
| LVIDs/BSA (mm/m 2 ) | 19.1 ± 2 | 18.3 ± 1 ‡ |
| LV length (cm) | 9.4 ± 0.6 | 9.4 ± 0.7 |
| LV length/BSA (cm/m 2 ) | 5.2 ± 0.4 | 4.9 ± 0.4 ‡ |
| LVEDV (mL) | 182 ± 21 | 172 ± 25 ∗ |
| LVEDV/BSA (mL/m 2 ) | 101 ± 10 | 89 ± 13 ‡ |
| Interventricular septum (mm) | 7.7 ± 1 | 9.4 ± 1 ‡ |
| Posterior wall (mm) | 8.4 ± 1 | 9.7 ± 1 ‡ |
| Wall thickness (average) (mm) | 8.1 ± 1 | 9.5 ± 1 ‡ |
| Wall thickness/BSA (mm/m 2 ) | 4.5 ± 1 | 4.9 ± 1 ‡ |
| LV mass (g) | 159 ± 20 | 209 ± 26 ‡ |
| LV mass/BSA (g/m 2 ) | 88 ± 11 | 108 ± 13 ‡ |
| Relative wall thickness | 0.32 ± 0.04 | 0.37 ± 0.04 ‡ |
LV Systolic Function
Parameters characterizing LV systolic function are shown in Table 3 . In the context of higher indexed LVEDV, runners demonstrated larger indexed stroke volumes than rowers (57 ± 6 vs 52 ± 8 mL/m 2 ; P < .001) ( Table 3 ). In contrast, LV ejection fraction and numerous complementary indices of LV systolic function, including average longitudinal systolic tissue velocity (S′), longitudinal and circumferential strain, apical and basal rotation, and LV twist, were not different between the two groups ( Table 3 ).
| Variable | Runners ( n = 40) | Rowers ( n = 40) |
|---|---|---|
| Ejection fraction (%) | 56 ± 5 | 58 ± 4 |
| Stroke volume (mL) | 102 ± 13 | 100 ± 15 |
| Stroke volume/BSA (mL/m 2 ) | 57 ± 6 | 52 ± 8 † |
| S′ lateral (cm/sec) | 7.4 ± 1 | 7.5 ± 1 |
| S′ septal (cm/sec) | 6.5 ± 1 | 6.9 ± 1 ∗ |
| S′ average (cm/sec) | 7.0 ± 1 | 7.3 ± 1 |
| Average longitudinal strain (%) | −21.0 ± 2 | −20.6 ± 2 |
| Average circumferential strain (%) | −23.8 ± 3 | −23.4 ± 3 |
| Basal rotation (°/sec) | −5.5 ± 3 | −5.3 ± 3 |
| Apical rotation (°/sec) | 16.1 ± 6 | 15.4 ± 7 |
| Twist, (°/sec) | 21.1 ± 7 | 20.3 ± 8 |
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