Physiology & Biochemistry
987
Right Ventricular Myocardial Responses to Progressive Exercise in Young Adult Males
Affiliations
Key words ▶ stress testing ● ▶ heart function ● ▶ echocardiography ●
accepted after revision January 02, 2014 Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1367047 Published online: May 16, 2014 Int J Sports Med 2014; 35: 987–993 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0172-4622 Correspondence Dr. Thomas Rowland Pediatrics Baystate Medical Center 759 Chestnut St. Springfield 01199 United States Tel.: + 1/413/794 7349 Fax: + 1/413/794 7140 [email protected]
T. Rowland1, M. Wharton2, T. Masters2, M. Mozer2, M. Santiago2, D. L. Smith2 1 2
Baystate Medical Center, Pediatrics, Springfield, United States Skidmore College, Department of Health and Exercise Sciences, Saratoga Springs, United States
Abstract Recent attention has been focused on possible unique features of the right ventricular response to exercise. This study investigated a) the responses of right ventricular cardiac dynamics and myocardial function to a standard bout of progressive cycle exercise in healthy young males, and b) the effect of level of aerobic fitness on these responses. 14 athletically-trained males (20.4 ± 1.5 years) and 11 normally-active males (21.1 ± 1.3 years) underwent a progressive upright cycle test to exhaustion with measurement of gas exchange variables and assessment of right ventricular stroke volume, systolic and diastolic myocardial velocities, and tricuspid inflow velocities by standard Doppler echocardiographic techniques at rest, submaximal and
peak exercise. Stroke volume rose initially by approximately 27 % in each group, followed by stable values to exhaustion. Values of maximal stroke index and maximal oxygen uptake were significantly greater in the trained group than the normally-active males (62 ± 10 ml m − 2, 54.3 ± 4.0 ml kg − 1 min − 1; 49 ± 7 ml m − 2, 40.3 ± 5.6 ml kg − 1 min − 1, respectively). No significant differences were observed in increases in systolic or diastolic myocardial velocities, peak pulmonary outflow velocity, systolic ejection rate, or tricuspid inflow velocity between the 2 groups. The magnitude of change of these variables was similar to those previously described for left ventricular responses to similar exercise. This study revealed no unique features of right ventricular functional responses to an acute exercise challenge in young males.
According to Poiseuille’s Law, augmentation of circulatory flow (Q) to meet the aerobic demands of endurance exercise is effected by Q ~ P/R, a fall in peripheral vascular resistance (R) accompanied by maintenance of the intravascular pressure head (P) by the cardiac pump [21]. The latter is comprised of 2 pumps operating in series, a small, thin-walled right ventricle pumping into a low-pressure, low-resistance pulmonary circulation and a larger, thick-walled left ventricle which ejects blood into a high-pressure, highresistance systemic circulation. The outputs of these 2 pumps over time must, by necessity, be equal. As the ventricle a) immediately responsible for generating systemic blood flow and b) more accessible to noninvasive diagnostic techniques, left ventricular function has traditionally been the focus of considerations of cardiac responses to endurance exercise. Growing evidence indicates, however, that functional responses to acute endurance exercise and chronic adaptations to endurance training may differ between the 2
sides of the heart [8, 10, 12]. The right ventricle possesses a unique anatomy, geometry, and myocardial contractile pattern compared to the left ventricle [10]. Most specifically pertinent to exercise responses, the relative reduction in downstream vascular resistance in the pulmonary vascular bed with dynamic exercise is lower and the relative augmentation of pulmonary artery pressure greater than that observed in the systemic circulation [12]. These features may expose the right ventricle to greater wall stress during endurance exercise [8], which could translate in turn to a greater susceptibility to myocardial fatigue and diminished contractile reserve compared to the left ventricle. Numerous reports have indicated findings consistent with transient myocardial dysfunction of both right and left ventricles in highly-trained athletes following extended competitions (see Oxborough et al. [16] for review). Recent findings suggest, however, that depressive effects evident on the ventricular myocardium following sustained high levels of cardiac output in such ath-
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Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
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Authors
letes may be disproportionately greater on the right side of the heart and characterized by unexpected right ventricular dilation [6, 15, 17]. It has been speculated, too, that chronic changes associated with such exaggerated right ventricular stresses with exercise might eventuate in permanent right ventricular dysfunction, accompanied by increased ventricular arrhythmogenicity and risk for sudden cardiac death in highly trained endurance athletes [23]. While such information has triggered increased interest in understanding normal right ventricular functional responses to dynamic exercise, previous studies have provided limited insights. In 2 studies, La Gerche and colleagues measured right ventricular longitudinal velocities by tissue Doppler imaging (TDI-S) during maximal or near-maximal semisupine exercise [9]. Values approximately doubled in both studies, similar to responses observed in the left ventricle. In another study, these investigators demonstrated great levels of right ventricular wall stress during an acute exercise bout compared to that of the left ventricle [8]. Measurements of increasing right ventricular strain and strain rates reflecting normal augmentation of systolic function have been reported during mild-moderate exercise intensities [9, 36]. Bossone et al. described similar patterns of right ventricular stroke volume response to submaximal supine exercise in hockey players and non-athletes [2]. Echocardiographic techniques which have permitted insights into myocardial function have been described in evaluating left ventricular responses to exercise in both non-trained and athletic populations [22, 25, 30]. This study utilized these same techniques to examine the normal cardiac dynamics and myocardial functional responses of the right ventricle to a standard acute bout of progressive, maximal, upright cycle exercise. The goals of this investigation were 3-fold: 1) Provide normative data describing right ventricular myocardial longitudinal velocities as markers of systolic and diastolic function during exercise as indicated by tissue Doppler imaging. 2) Compare measures of global ventricular inotropic function (systolic ejection rate, pattern of stroke volume response, peak pulmonary artery velocity) of the right ventricle during progressive exercise to exhaustion with those previously described for the left ventricle. 3) Examine the influence of aerobic fitness across a moderate range of maximal oxygen uptake (VO2max) on right ventricular inotropic and lusitropic responses to exercise.
Methods
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14 athletically-trained college-age males (20.4 ± 1.5 years) and 11 non-trained active college-age males (21.1 ± 1.3 years) volunteered for exercise testing. 10 of the highly trained participants were varsity athletes (soccer, lacrosse, swimming, basketball) at a NCAA Division III institution and 4 others engaged in fitness activities (cycling, running, cross-country skiing) 4–5 times weekly. Normally active participants reported little regular planned exercise ( < 3 days per week). None of the participants were regular smokers (one of the normally active men reported “occasional” smoking). All subjects were in good health and had no known cardiovascular disease or deficiencies. Prior to testing, participants completed an informed consent form and health history questionnaire in order to screen for potential risks, and all participants were screened by a medical
professional prior to testing. Informed consent was obtained from all participants at the outset of the study. The study was approved by the Institutional Review Board at Skidmore College. This study meets the ethical standards of the International Journal of Sports Medicine [5]. Body height was obtained to the nearest 0.01 m using a stadiometer (SECA) and weight was measured to the nearest 0.1 kg using an electronic scale (Health-O-Meter). The dual energy X-Ray absorptiometry (DXA) technique was used to estimate percent body fat (iDXA, GE Lunar, Madison, WI). Prior to exercise testing, a screening 2-dimensional echocardiogram with Doppler velocity and color flow was performed with subjects in the supine left lateral position to assure absence of heart disease and indication of pulmonary hypertension. All echocardiographic studies at rest and during exercise in this investigation were performed with an Aloka SDD model 5 500 (Tokyo, Japan) using a 2.5 MHz transducer. Participants performed a graded exercise test to volitional fatigue on a Monark Ergomedic 828 E cycle ergometer. Prior to testing, participants were familiarized with the protocol and testing devices. All participants were instructed to (a) refrain from strenuous exercise and alcohol during the 24 h preceding testing, (b) abstain from food intake within 2 h of testing session, and (c) consume sufficient fluids during the 24 h preceding testing to ensure that they were normally hydrated. A urine specific gravity measure was obtained prior to testing to ensure that all participants were tested in a euhydrated state (USG < 1.020). Exercise was performed on a cycle ergometer at a constant cadence of 60 rpm. Initial and incremental workloads were 37.5 watts with stage duration of 3 min. Heart rate was monitored at each minute during exercise, and blood pressure was obtained by the standard auscultatory technique during the last minute of each stage. Expired gases were collected throughout the protocol using a metabolic cart system (Parvomedics, UT). The test was terminated when the participant indicated he could no longer continue or could not maintain the cadence. Tests were considered maximal if at least 2 of the following criteria were met: (a) respiratory exchange ratio (RER) ≥ 1.10, (b) plateau in oxygen uptake despite increase in workload, and (c) heart rate within 12 beats of age-predicted maximum values [19]. Heart rate was measured electrocardiographically. Stroke volume was estimated as the product of the cross-sectional area of the pulmonary valve annulus (measured at rest) and the velocity-time integral (VTI) of blood flow across the valve, measured by pulse wave Doppler in a parasternal short axis view. The former was calculated from the diameter of the valve ring measured from the hinge points of the leaflets at maximal excursion in the parasternal short axis view during forced end-expiration (to provide identification of the lateral wall) with the subject sitting upright on the cycle ergometer. Mean value of valve diameter was calculated from 3–4 consistent measurements. Beat-to-beat velocity-time curves were traced off-line to determine the mean VTI of the 3–8 consistently highest values. In this computation of stroke volume, the pulmonary valve ring in the upright position was considered to be circular with minimal change in average diameter during ventricular systole as exercise intensity increased. Cardiac output was calculated as the product of heart rate and stroke volume. Cardiac output and stroke volume were indexed to body surface area as cardiac index and stroke index, respectively.
Rowland T et al. Right Ventricular Responses to Exercise… Int J Sports Med 2014; 35: 987–993
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988 Physiology & Biochemistry
Physiology & Biochemistry
70 65 Stroke index (mL.m– 2)
60 55 50 45 40 35 30
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 1 Right ventricular stroke index responses to progressive upright cycle exercise in aerobically-trained subjects (N = 14) and untrained, normally active young adult males (N = 11). Dashed line connects to average maximal value vs. mean work time. Group values are significantly different (P < 0.05) for all workload comparisons.
Results
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Average body mass for the trained subjects was 76 ± 8 kg, height 176 ± 5 cm, body surface area 1.9 ± 0.1 m2, and percent body fat 15.3 ± 3.1 %. Respective values for the normally active group were 80 ± 10 kg, 182 ± 7 cm, 2.01 ± 0.1 m2, and 20.6 ± 6.7 %. Screening echocardiograms revealed no evidence of structural or functional heart disease, particularly right ventricular outflow obstruction, in all subjects. Trivial or mild tricuspid regurgitation was identified in 13 (52 %) of the subjects. In no case did the regurgitant jet velocity exceed 2.5 ms, implying no evidence of elevation of resting pulmonary artery pressure in any subject. All subjects satisfied criteria for a maximal test. Peak heart rates for the aerobically-trained and non-trained subjects (180 ± 9 and 182 ± 16 bpm, respectively, p > 0.05) and RERmax (1.16 ± 0.09 and 1.24 ± 0.10, respectively, p > 0.05) were not significantly different, indicating an equal maximal effort during cycle exercise testing. The trained subjects demonstrated a greater VO2max compared to the untrained (54.3 ± 4.0 ml kg − 1 min − 1 and 40.3 ± 5.6 ml kg − 1 min − 1, respectively, p < 0.05). Complete batteries of echocardiographic measures during exercise were obtained in all subjects. Resting and maximal stroke index values were significantly greater in the aerobically-trained group compared to the non-trained group (47 ± 13 vs. 38 ± 13 ml m − 2 and 62 ± 10 vs. 49 ± 7 ml m − 2, respectively) (P < 0.05). Maximal-to-rest ratios of stroke index, however, were similar (1.32 for the trained and 1.29 for the untrained). The pattern of stroke volume response was similar in both groups, with an initial early rise of approximately 27 % and then little change at higher work intensities. Stroke index values were significantly higher values ▶ Fig. 1). in the trained subjects at rest and all levels of exercise (● Maximal cardiac index was 11.1 ± 1.7 L min − 1 m − 2 in the trained and 8.9 ± 1.2 L min − 1 m − 2 in the untrained (P < 0.05). Systolic and diastolic functional variables at rest and maximal exercise for the trained and untrained subjects are outlined ▶ Table 1. With the exception of E/E’, all rose progressively in ● during exercise with increases ranging from factors of 1.9 to 3.2
Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
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Tricuspid peak early diastolic inflow velocity (E wave) was recorded in the apical 4-chamber view by pulse wave Doppler. Values were recorded as the mean of the highest 3–8 consistent velocity measures. Late diastolic velocity (A wave) was not considered, as this wave was observed to merge with the E wave beginning at low exercise intensities. Pulse wave tissue Doppler imaging (TDI) was performed at the lateral aspect of the tricuspid valve annulus in the apical 4 chamber view to record longitudinal right ventricular myocardial velocities in both systole (TDI-S) and diastole (TDI-E’). Transducer alignment was considered appropriate when the ventricular septum was vertical. Values were again recorded and averaged as the highest 3–8 consistently greatest velocities. Echocardiographic images for this battery of variables were recorded at rest, beginning at 1:30 in each submaximal exercise stage, and during the final minute of exercise for determination of peak values. All recordings (except pulmonary valve diameter) were obtained during spontaneous respirations. Measurements were determined off-line. Because of this limited time “window” during exercise, measurement of echocardiographic variables was restricted to those of the right ventricle. Results were compared to those of previously published exercise studies of left ventricular responses which utilized a) identical techniques, b) a similar age group, and c) the same exercise model. Duration of ventricular ejection time was measured from the width of the velocity-time curve. Peak pulmonary artery velocity was defined as the apex of the velocity-time curve. Systolic myocardial function was assessed by peak pulmonary outflow velocity, systolic ejection rate (stroke volume divided by systolic ejection time), TDI-S, and the pattern of stroke volume response. Diastolic function was examined by E peak velocity (reflecting upstream right atrial-to-downstream ventricular pressure gradient during early diastolic filling), TDI-E’ velocity (ventricular longitudinal myocardial relaxation properties), and E/E’ (right ventricular filling pressure). These measures have all been well-validated as reliable markers of left ventricular inotropic and lusitropic function [3, 14, 35]. While less documentation exists for examining right ventricular function, the limited available data support similar utility of these measures in assessing the right side of the heart [32]. Values of TDI-S at the lateral tricuspid annulus correlate with right ventricular ejection fraction determined both by radionuclide angiography [11, 33] and magnetic resonance imaging [36]. Values of right-sided E/E’ correspond to measures of right ventricular filling pressure obtained at cardiac catheterization [13]. E/E’ has been utilized as an echocardiographic marker of right atrial pressure [4] based on the work of Said et al. [34]. SPSS version 20 was used for statistical analyses (SPSS inc., Chicago, Il). Results were expressed as mean ± standard deviation. Anthropometric values, resting ventricular dimensions and hemodynamic variables at rest and at maximal exercise were compared between the 2 groups by an independent t-test. The Greenhouse-Geisser test was performed to verify normal distribution of the data. The significance of changes in echocardiographic data during exercise was examined using a 2-way ANOVA (group × time) with repeated measures on time. When appropriate, main effects significance was examined using post hoc comparisons by Bonferroni-corrected t-tests. Statistical significance was defined as P < 0.05.
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990 Physiology & Biochemistry
Aerobically-
reports Left
trained
ventricle*
20 10 0 –10
106 181 1.70 208 373 1.79
–20 –30 –40 –50 –60
9 20 2.2
0
3
6
9 12 Time (min)
Aerobically trained 73 153 2.1 10 24 2.4
21
Normally active
3.7 3.5 3.3 3.1 2.9 2.7 2.5 2.3 2.1
Discussion
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This study supplies information regarding normal functional responses of the right ventricle in healthy young men to upright exercise on a progressive maximal cycle test. The findings a) provide normative data for such responses as measured by standard echocardiographic techniques, b) indicate certain differences in numerical values of functional markers compared to those previously reported for the left ventricle but equivalent magnitudes of response, and c) reveal no relationship of aerobic fitness (within a moderate range) to right ventricular myocardial functional responses to an acute bout of progressive exercise. Within this model of acute exercise, then, no evidence was observed of unique right ventricular myocardial responses or fatigue. With increasing work loads right ventricular stroke volume was observed to initially rise by approximately 27 % in both groups and then remained essentially stable to maximal exercise. This pattern of “plateau” of stroke volume is identical to that consistently observed in assessment of left ventricular responses to progressive cycle exercise performed in the upright position
18
3.9
7.4 6.5 0.88
▶ Fig. 2–5). No significant differences were observed in these (● measures between the 2 groups, nor was any group × time interaction seen for any exercise variable (except for a minor interaction for E’).
15
Fig. 2 Tissue Doppler-S and E’ velocities, reflecting right ventricular systolic and diastolic function, respectively, during progressive exercise in aerobically-trained and untrained men. P > 0.05 for all group comparisons.
E / E’
Systolic function Peak pulmonary outflow velocity (cm s − 1) Rest 84 (11) 95 (15) Max 170 (17) 183 (12) Δ factor 2.02 1.93 Systolic ejection rate (ml s − 1) Rest 304 (39) 327 (51) Max 669 (110) 715 (98) Δ factor 2.20 2.19 TDI-S (cm s − 1) Rest 12 (3) 13 (3) Max 33 (8) 34 (5) Δ factor 2.8 2.6 Diastolic function Diastolic filling (E) (cm s − 1) Rest 51 (12) 49 (8) Max 121 (19) 135 (22) Δ factor 2.4 2.8 TDI-E’ (cm s − 1) Rest 16 (4) 15 (3) Max 42 (6) 49 (9) Δ factor 2.6 3.3 E/E’ Rest 3.26 (0.89) 3.31 (0.92) Max 2.88 (0.33) 2.87 (0.69) Δ factor 0.88 0.87
30
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 3 Right ventricular filling pressure estimated by E/E’ obtained by Doppler echocardiography during maximal progressive exercise in aerobically-trained and non-trained men. P > 0.05 for all group comparisons.
[21]. The initial increase has been attributed to mobilization of blood sequestered in the lower extremity when assuming the upright position. Other than this initial “refilling” phenomenon, then, stroke volume changes little during the course an acute bout of progressive exercise. Occurring concomitantly with a 3–4 fold rise in systemic venous return to the heart, this stability of stroke volume is explained by the rise in heart rate, which matches venous return and maintains a constant ventricular filling volume. It is evident, then, that the rise in ventricular inotropic and lusitropic function in such exercise serves to maintain stroke volume as the ejection time shortens.
Rowland T et al. Right Ventricular Responses to Exercise… Int J Sports Med 2014; 35: 987–993
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Non-trained
Previous
E’ (cm.s– 1)
Present study
40 S (cm.s– 1)
Table 1 Echocardiographic variables in the present study evaluating right ventricular function compared to previously published data assessing those of the left ventricle. Values are mean (standard deviation). No significant group or group-time interaction was observed except for group-time interaction for TDI-E’. *Left ventricular values are averages from multiple published sources in young, non-athletic subjects (see text for references).
200
POV (cm.s–1)
180 160 140 120 100 80 60
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 4 Peak pulmonary outflow velocities during progressive upright cycle in trained and non-trained men. P > 0.05 for all group comparisons.
840
Ejection rate (mL.s– 1)
740 640 540 440 340 240 140 40
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 5 Systolic ejection rate (stroke volume divided by systolic ejection time) during maximal exercise testing of aerobically-trained and nontrained men. P > 0.05 for all group comparisons.
The pattern of rise in the stroke volume in this study then indicates that a similar scenario occurs in the right ventricle. It also implies an appropriate augmentation of myocardial systolic and diastolic responses, since any dysfunctional response to this exercise model would be evidenced by a decline in stroke volume as work intensity increased [27]. Normal systolic and diastolic response to exercise in these subjects equivalent to those previously observed in the left ventricle is supported by the changes observed in other functional mark▶ Table 1. The values outlined in this table are ers outlined in ● compared to the average of resting and maximal values of previous reports assessing left ventricular function during upright or semi-supine cycle exercise to exhaustion in young nonathletic subjects. (References for average values for markers of left ventricular systolic function can be accessed in the review by Rowland and Unnithan [28], for mitral E [3, 24, 26, 29–31], and TDI-E’ [1, 9, 29–31]). Maximal-to-rest ratio for these variables in the present study ranged from 1.9 (systolic ejection rate) to 3.3 (TDI-E’), delta fac-
tors which are similar to or slightly greater than those previously described for left ventricular systolic and diastolic responses. However, certain specific absolute values at rest and during exercise are observed to vary from those reported for the left ventricle. Differences in longitudinal systolic (TDI-S) and diastolic (TDI-E’) values can be explained by the unique fiber orientation and contractile pattern of the right compared to the left ventricle [10]. Compared to the left ventricle, the right is a thin-walled (3–5 mm) crescent-shaped structure composed of 3 compartments, the inlet and apex (comprising the trabeculated sinus portion), and a smooth-walled outlet, or infundibulum. Contraction of the right ventricle starts inferiorly in the sinus and proceeds in a peristaltic motion towards the infundibulum, while the thick walled left ventricle contracts by a “wringing out” motion of helically-oriented, spiral fibers. In contrast to the left ventricle, too, the fibers of the right ventricular free wall are oriented primarily in a longitudinal direction, accounting for greater myocardial velocities with Doppler imaging. Lower peak velocities were recorded at rest and during exercise for diastolic tricuspid inflow (E) compared to previous experience with trans-mitral velocities. This mimics the findings of Zoghbi et al., who reported 22 % lower peak E velocities during tricuspid inflow compared to those at the mitral valve at rest [37]. E velocity reflects the gradient between upstream (right atrial) and downstream (right ventricular) pressure, which accounts for ventricular filling. During exercise, the former is dictated largely by heart rate (rising to match systemic venous return), while the latter is influenced by myocardial relaxation properties as well as ventricular post-systolic elastic recoil [21]. The normally-maintained stroke volume, expected max:rest E ratio and unchanged right ventricular filling pressure (as indicated by E/E’) imply that the balance of these 2 influences during exercise in this study was normal. Zoghbi et al. noted that a larger flow area of the tricuspid annulus compared to that of the mitral valve might be at least partly responsible for lower E velocities recorded in right ventricular inflow [37]. E/E’, an indicator of ventricular filling pressure, did not change significantly during the course of exercise, consistent with left ventricular studies that indicate a stable left ventricular end diastolic volume and close matching of rise in heart rate with augmented pulmonary venous return [24]. The pattern of E/E’ also mimicked that of previous left ventricular reports during upright exercise, with a small early rise as systemic venous return increases when blood is mobilized from dependent legs (Frank Starling effect), followed by a gradual decline to exercise exhaustion. The latter is consistent with a small but progressive decrease in left ventricular end diastolic dimension observed by echocardiography [20, 24]. In the present study, this can be presumed to reflect similar trends in right ventricular size during progressive exercise. No significant differences were observed in markers of systolic or diastolic function during exercise between the trained and non-trained subjects. This study thus provides evidence that within a moderate range of aerobic fitness, VO2max is independent of right ventricular myocardial functional responses to exercise. This finding is consistent with reports of left ventricular dynamics during the same exercise model [25, 30]. Instead, the primary factors which dictate individual variations in VO2max within the moderate range are those which influence ventricular diastolic size, including genetic pre-disposition, blood vol-
Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
991
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Physiology & Biochemistry
ume, and resting bradycardia (by increasing ventricular filling time) [18]. Within the range of aerobic fitness included in this study, there is no evidence that either left or right ventricular inotropic or lusitropic functional responses to exercise contribute to individual variations in VO2max. La Gerche et al. supported this conclusion in a group of 55 subjects (comprised of 40 athletes and 15 non-athletes) whose mean VO2max was 51.4 ± 11.9 ml kg − 1 min − 1 with a range from 23.5 to 82.2 ml kg − 1min − 1 [7]. Semi-supine exercise was performed to an average heart rate of 177 bpm. Multivariate analysis revealed that tissue Doppler measures of systolic and diastolic function did not predict VO2max, which instead was related significantly only to resting right ventricular volume and left ventricular mass. Several limitations of this study should be noted. No direct comparisons of right ventricular functional responses to exercise were made with left ventricular responses. Test-retest reliability was not assessed. It was assumed that respiratory influences on right-sided flow velocities during exercise were minor. Findings were limited to young males within a limited range of aerobic fitness, and results cannot be assumed to reflect those in comparisons of subjects with low aerobic fitness and elite level endurance athletes.
Conclusions
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While the right ventricle may face a greater after-load during exercise than the left, no evidence was provided by this study of any perturbations from expected myocardial systolic or diastolic functional responses to an acute progressive exercise challenge. No differences were observed in right ventricular responses to progressive exercise between trained and untrained subjects, providing evidence suggesting that ventricular size rather than function is responsible for dictating level of aerobic fitness, at least within the moderate range of the study groups. This study supported the feasibility of utilizing standard Doppler echocardiographic techniques in examining right ventricular functional responses to exercise. With this method, future research can address the importance of such responses in both clinical assessment of patients with heart disease as well as the effects of high levels of training and competition in elite endurance athletes.
Acknowledgements
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The authors wish to express their gratitude to Prof. Patricia C. Fehling for her invaluable contributions to this study as well as to the enthusiastic subjects who volunteered to participate. Funding for this study was provided from the Student Opportunity Fund at Skidmore College.
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Physiology & Biochemistry
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approach: comparison with cardiac magnetic resonance imaging. J Am Soc Echocardiogr 2009; 22: 361–368 Said K, Shehata A, Ashour Z, El-Tobgi S. Value of conventional and tissue Doppler echocardiography in the nonvasive measurement of right atrial pressure. Echocardiography 2012; 29: 779–784 Sohn D-W, Chaie L-H, Lee D-J. Assessment of mitral annulus velocity by Doppler tissue imaging in the evaluation of left ventricular diastolic function. J Am Coll Cardiol 1997; 30: 474–480 Yang HS, Mookadam F, Warsame TA, Khandheria BK, Tajik JA, Chandrasekaran K. Evaluation of right ventricular global and regional function during stress echocardiography using novel velocity vector imaging. Eur J Echocardiogr 2010; 11: 157–164 Zoghbi WA, Habib GB, Quionones MA. Doppler assessment of right ventricular filling in a normal population. Comparison with left ventricular filling dynamics. Circulation 1990; 82: 1316–1324
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28 Rowland T, Unnithan V. Myocardial response to progressive exercise in healthy subjects: a review. Curr Sports Med Rep 2013; 12: 93–100 29 Rowland T, Unnithan V, Barker P, Lindley M, Roche D, Garrard M. Time of day effect on cardiac responses to progressive exercise. Chronobiol Int 2011; 28: 611–616 30 Rowland T, Unnithan V, Roche D, Garrard M, Holloway K, Marwood S. Myocardial function and aerobic fitness in adolescent females. Eur J Appl Physiol 2011; 111: 1991–1997 31 Rowland T, Willers M. Reproducibility of Doppler measures of ventricular function during maximal upright cycling. Cardiol Young 2010; 20: 676–679 32 Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography. J Am Soc Echocardiogr 2010; 23: 685–713 33 Sade LE, Hulmez O, Ozyer U, Ozgul E, Agildere M, Muderrisoglu H. Tissue Doppler study of the right ventricle with a multisegmental
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987
Right Ventricular Myocardial Responses to Progressive Exercise in Young Adult Males
Affiliations
Key words ▶ stress testing ● ▶ heart function ● ▶ echocardiography ●
accepted after revision January 02, 2014 Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1367047 Published online: May 16, 2014 Int J Sports Med 2014; 35: 987–993 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0172-4622 Correspondence Dr. Thomas Rowland Pediatrics Baystate Medical Center 759 Chestnut St. Springfield 01199 United States Tel.: + 1/413/794 7349 Fax: + 1/413/794 7140 [email protected]
T. Rowland1, M. Wharton2, T. Masters2, M. Mozer2, M. Santiago2, D. L. Smith2 1 2
Baystate Medical Center, Pediatrics, Springfield, United States Skidmore College, Department of Health and Exercise Sciences, Saratoga Springs, United States
Abstract Recent attention has been focused on possible unique features of the right ventricular response to exercise. This study investigated a) the responses of right ventricular cardiac dynamics and myocardial function to a standard bout of progressive cycle exercise in healthy young males, and b) the effect of level of aerobic fitness on these responses. 14 athletically-trained males (20.4 ± 1.5 years) and 11 normally-active males (21.1 ± 1.3 years) underwent a progressive upright cycle test to exhaustion with measurement of gas exchange variables and assessment of right ventricular stroke volume, systolic and diastolic myocardial velocities, and tricuspid inflow velocities by standard Doppler echocardiographic techniques at rest, submaximal and
peak exercise. Stroke volume rose initially by approximately 27 % in each group, followed by stable values to exhaustion. Values of maximal stroke index and maximal oxygen uptake were significantly greater in the trained group than the normally-active males (62 ± 10 ml m − 2, 54.3 ± 4.0 ml kg − 1 min − 1; 49 ± 7 ml m − 2, 40.3 ± 5.6 ml kg − 1 min − 1, respectively). No significant differences were observed in increases in systolic or diastolic myocardial velocities, peak pulmonary outflow velocity, systolic ejection rate, or tricuspid inflow velocity between the 2 groups. The magnitude of change of these variables was similar to those previously described for left ventricular responses to similar exercise. This study revealed no unique features of right ventricular functional responses to an acute exercise challenge in young males.
According to Poiseuille’s Law, augmentation of circulatory flow (Q) to meet the aerobic demands of endurance exercise is effected by Q ~ P/R, a fall in peripheral vascular resistance (R) accompanied by maintenance of the intravascular pressure head (P) by the cardiac pump [21]. The latter is comprised of 2 pumps operating in series, a small, thin-walled right ventricle pumping into a low-pressure, low-resistance pulmonary circulation and a larger, thick-walled left ventricle which ejects blood into a high-pressure, highresistance systemic circulation. The outputs of these 2 pumps over time must, by necessity, be equal. As the ventricle a) immediately responsible for generating systemic blood flow and b) more accessible to noninvasive diagnostic techniques, left ventricular function has traditionally been the focus of considerations of cardiac responses to endurance exercise. Growing evidence indicates, however, that functional responses to acute endurance exercise and chronic adaptations to endurance training may differ between the 2
sides of the heart [8, 10, 12]. The right ventricle possesses a unique anatomy, geometry, and myocardial contractile pattern compared to the left ventricle [10]. Most specifically pertinent to exercise responses, the relative reduction in downstream vascular resistance in the pulmonary vascular bed with dynamic exercise is lower and the relative augmentation of pulmonary artery pressure greater than that observed in the systemic circulation [12]. These features may expose the right ventricle to greater wall stress during endurance exercise [8], which could translate in turn to a greater susceptibility to myocardial fatigue and diminished contractile reserve compared to the left ventricle. Numerous reports have indicated findings consistent with transient myocardial dysfunction of both right and left ventricles in highly-trained athletes following extended competitions (see Oxborough et al. [16] for review). Recent findings suggest, however, that depressive effects evident on the ventricular myocardium following sustained high levels of cardiac output in such ath-
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Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
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Authors
letes may be disproportionately greater on the right side of the heart and characterized by unexpected right ventricular dilation [6, 15, 17]. It has been speculated, too, that chronic changes associated with such exaggerated right ventricular stresses with exercise might eventuate in permanent right ventricular dysfunction, accompanied by increased ventricular arrhythmogenicity and risk for sudden cardiac death in highly trained endurance athletes [23]. While such information has triggered increased interest in understanding normal right ventricular functional responses to dynamic exercise, previous studies have provided limited insights. In 2 studies, La Gerche and colleagues measured right ventricular longitudinal velocities by tissue Doppler imaging (TDI-S) during maximal or near-maximal semisupine exercise [9]. Values approximately doubled in both studies, similar to responses observed in the left ventricle. In another study, these investigators demonstrated great levels of right ventricular wall stress during an acute exercise bout compared to that of the left ventricle [8]. Measurements of increasing right ventricular strain and strain rates reflecting normal augmentation of systolic function have been reported during mild-moderate exercise intensities [9, 36]. Bossone et al. described similar patterns of right ventricular stroke volume response to submaximal supine exercise in hockey players and non-athletes [2]. Echocardiographic techniques which have permitted insights into myocardial function have been described in evaluating left ventricular responses to exercise in both non-trained and athletic populations [22, 25, 30]. This study utilized these same techniques to examine the normal cardiac dynamics and myocardial functional responses of the right ventricle to a standard acute bout of progressive, maximal, upright cycle exercise. The goals of this investigation were 3-fold: 1) Provide normative data describing right ventricular myocardial longitudinal velocities as markers of systolic and diastolic function during exercise as indicated by tissue Doppler imaging. 2) Compare measures of global ventricular inotropic function (systolic ejection rate, pattern of stroke volume response, peak pulmonary artery velocity) of the right ventricle during progressive exercise to exhaustion with those previously described for the left ventricle. 3) Examine the influence of aerobic fitness across a moderate range of maximal oxygen uptake (VO2max) on right ventricular inotropic and lusitropic responses to exercise.
Methods
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14 athletically-trained college-age males (20.4 ± 1.5 years) and 11 non-trained active college-age males (21.1 ± 1.3 years) volunteered for exercise testing. 10 of the highly trained participants were varsity athletes (soccer, lacrosse, swimming, basketball) at a NCAA Division III institution and 4 others engaged in fitness activities (cycling, running, cross-country skiing) 4–5 times weekly. Normally active participants reported little regular planned exercise ( < 3 days per week). None of the participants were regular smokers (one of the normally active men reported “occasional” smoking). All subjects were in good health and had no known cardiovascular disease or deficiencies. Prior to testing, participants completed an informed consent form and health history questionnaire in order to screen for potential risks, and all participants were screened by a medical
professional prior to testing. Informed consent was obtained from all participants at the outset of the study. The study was approved by the Institutional Review Board at Skidmore College. This study meets the ethical standards of the International Journal of Sports Medicine [5]. Body height was obtained to the nearest 0.01 m using a stadiometer (SECA) and weight was measured to the nearest 0.1 kg using an electronic scale (Health-O-Meter). The dual energy X-Ray absorptiometry (DXA) technique was used to estimate percent body fat (iDXA, GE Lunar, Madison, WI). Prior to exercise testing, a screening 2-dimensional echocardiogram with Doppler velocity and color flow was performed with subjects in the supine left lateral position to assure absence of heart disease and indication of pulmonary hypertension. All echocardiographic studies at rest and during exercise in this investigation were performed with an Aloka SDD model 5 500 (Tokyo, Japan) using a 2.5 MHz transducer. Participants performed a graded exercise test to volitional fatigue on a Monark Ergomedic 828 E cycle ergometer. Prior to testing, participants were familiarized with the protocol and testing devices. All participants were instructed to (a) refrain from strenuous exercise and alcohol during the 24 h preceding testing, (b) abstain from food intake within 2 h of testing session, and (c) consume sufficient fluids during the 24 h preceding testing to ensure that they were normally hydrated. A urine specific gravity measure was obtained prior to testing to ensure that all participants were tested in a euhydrated state (USG < 1.020). Exercise was performed on a cycle ergometer at a constant cadence of 60 rpm. Initial and incremental workloads were 37.5 watts with stage duration of 3 min. Heart rate was monitored at each minute during exercise, and blood pressure was obtained by the standard auscultatory technique during the last minute of each stage. Expired gases were collected throughout the protocol using a metabolic cart system (Parvomedics, UT). The test was terminated when the participant indicated he could no longer continue or could not maintain the cadence. Tests were considered maximal if at least 2 of the following criteria were met: (a) respiratory exchange ratio (RER) ≥ 1.10, (b) plateau in oxygen uptake despite increase in workload, and (c) heart rate within 12 beats of age-predicted maximum values [19]. Heart rate was measured electrocardiographically. Stroke volume was estimated as the product of the cross-sectional area of the pulmonary valve annulus (measured at rest) and the velocity-time integral (VTI) of blood flow across the valve, measured by pulse wave Doppler in a parasternal short axis view. The former was calculated from the diameter of the valve ring measured from the hinge points of the leaflets at maximal excursion in the parasternal short axis view during forced end-expiration (to provide identification of the lateral wall) with the subject sitting upright on the cycle ergometer. Mean value of valve diameter was calculated from 3–4 consistent measurements. Beat-to-beat velocity-time curves were traced off-line to determine the mean VTI of the 3–8 consistently highest values. In this computation of stroke volume, the pulmonary valve ring in the upright position was considered to be circular with minimal change in average diameter during ventricular systole as exercise intensity increased. Cardiac output was calculated as the product of heart rate and stroke volume. Cardiac output and stroke volume were indexed to body surface area as cardiac index and stroke index, respectively.
Rowland T et al. Right Ventricular Responses to Exercise… Int J Sports Med 2014; 35: 987–993
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988 Physiology & Biochemistry
Physiology & Biochemistry
70 65 Stroke index (mL.m– 2)
60 55 50 45 40 35 30
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 1 Right ventricular stroke index responses to progressive upright cycle exercise in aerobically-trained subjects (N = 14) and untrained, normally active young adult males (N = 11). Dashed line connects to average maximal value vs. mean work time. Group values are significantly different (P < 0.05) for all workload comparisons.
Results
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Average body mass for the trained subjects was 76 ± 8 kg, height 176 ± 5 cm, body surface area 1.9 ± 0.1 m2, and percent body fat 15.3 ± 3.1 %. Respective values for the normally active group were 80 ± 10 kg, 182 ± 7 cm, 2.01 ± 0.1 m2, and 20.6 ± 6.7 %. Screening echocardiograms revealed no evidence of structural or functional heart disease, particularly right ventricular outflow obstruction, in all subjects. Trivial or mild tricuspid regurgitation was identified in 13 (52 %) of the subjects. In no case did the regurgitant jet velocity exceed 2.5 ms, implying no evidence of elevation of resting pulmonary artery pressure in any subject. All subjects satisfied criteria for a maximal test. Peak heart rates for the aerobically-trained and non-trained subjects (180 ± 9 and 182 ± 16 bpm, respectively, p > 0.05) and RERmax (1.16 ± 0.09 and 1.24 ± 0.10, respectively, p > 0.05) were not significantly different, indicating an equal maximal effort during cycle exercise testing. The trained subjects demonstrated a greater VO2max compared to the untrained (54.3 ± 4.0 ml kg − 1 min − 1 and 40.3 ± 5.6 ml kg − 1 min − 1, respectively, p < 0.05). Complete batteries of echocardiographic measures during exercise were obtained in all subjects. Resting and maximal stroke index values were significantly greater in the aerobically-trained group compared to the non-trained group (47 ± 13 vs. 38 ± 13 ml m − 2 and 62 ± 10 vs. 49 ± 7 ml m − 2, respectively) (P < 0.05). Maximal-to-rest ratios of stroke index, however, were similar (1.32 for the trained and 1.29 for the untrained). The pattern of stroke volume response was similar in both groups, with an initial early rise of approximately 27 % and then little change at higher work intensities. Stroke index values were significantly higher values ▶ Fig. 1). in the trained subjects at rest and all levels of exercise (● Maximal cardiac index was 11.1 ± 1.7 L min − 1 m − 2 in the trained and 8.9 ± 1.2 L min − 1 m − 2 in the untrained (P < 0.05). Systolic and diastolic functional variables at rest and maximal exercise for the trained and untrained subjects are outlined ▶ Table 1. With the exception of E/E’, all rose progressively in ● during exercise with increases ranging from factors of 1.9 to 3.2
Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
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Tricuspid peak early diastolic inflow velocity (E wave) was recorded in the apical 4-chamber view by pulse wave Doppler. Values were recorded as the mean of the highest 3–8 consistent velocity measures. Late diastolic velocity (A wave) was not considered, as this wave was observed to merge with the E wave beginning at low exercise intensities. Pulse wave tissue Doppler imaging (TDI) was performed at the lateral aspect of the tricuspid valve annulus in the apical 4 chamber view to record longitudinal right ventricular myocardial velocities in both systole (TDI-S) and diastole (TDI-E’). Transducer alignment was considered appropriate when the ventricular septum was vertical. Values were again recorded and averaged as the highest 3–8 consistently greatest velocities. Echocardiographic images for this battery of variables were recorded at rest, beginning at 1:30 in each submaximal exercise stage, and during the final minute of exercise for determination of peak values. All recordings (except pulmonary valve diameter) were obtained during spontaneous respirations. Measurements were determined off-line. Because of this limited time “window” during exercise, measurement of echocardiographic variables was restricted to those of the right ventricle. Results were compared to those of previously published exercise studies of left ventricular responses which utilized a) identical techniques, b) a similar age group, and c) the same exercise model. Duration of ventricular ejection time was measured from the width of the velocity-time curve. Peak pulmonary artery velocity was defined as the apex of the velocity-time curve. Systolic myocardial function was assessed by peak pulmonary outflow velocity, systolic ejection rate (stroke volume divided by systolic ejection time), TDI-S, and the pattern of stroke volume response. Diastolic function was examined by E peak velocity (reflecting upstream right atrial-to-downstream ventricular pressure gradient during early diastolic filling), TDI-E’ velocity (ventricular longitudinal myocardial relaxation properties), and E/E’ (right ventricular filling pressure). These measures have all been well-validated as reliable markers of left ventricular inotropic and lusitropic function [3, 14, 35]. While less documentation exists for examining right ventricular function, the limited available data support similar utility of these measures in assessing the right side of the heart [32]. Values of TDI-S at the lateral tricuspid annulus correlate with right ventricular ejection fraction determined both by radionuclide angiography [11, 33] and magnetic resonance imaging [36]. Values of right-sided E/E’ correspond to measures of right ventricular filling pressure obtained at cardiac catheterization [13]. E/E’ has been utilized as an echocardiographic marker of right atrial pressure [4] based on the work of Said et al. [34]. SPSS version 20 was used for statistical analyses (SPSS inc., Chicago, Il). Results were expressed as mean ± standard deviation. Anthropometric values, resting ventricular dimensions and hemodynamic variables at rest and at maximal exercise were compared between the 2 groups by an independent t-test. The Greenhouse-Geisser test was performed to verify normal distribution of the data. The significance of changes in echocardiographic data during exercise was examined using a 2-way ANOVA (group × time) with repeated measures on time. When appropriate, main effects significance was examined using post hoc comparisons by Bonferroni-corrected t-tests. Statistical significance was defined as P < 0.05.
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990 Physiology & Biochemistry
Aerobically-
reports Left
trained
ventricle*
20 10 0 –10
106 181 1.70 208 373 1.79
–20 –30 –40 –50 –60
9 20 2.2
0
3
6
9 12 Time (min)
Aerobically trained 73 153 2.1 10 24 2.4
21
Normally active
3.7 3.5 3.3 3.1 2.9 2.7 2.5 2.3 2.1
Discussion
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This study supplies information regarding normal functional responses of the right ventricle in healthy young men to upright exercise on a progressive maximal cycle test. The findings a) provide normative data for such responses as measured by standard echocardiographic techniques, b) indicate certain differences in numerical values of functional markers compared to those previously reported for the left ventricle but equivalent magnitudes of response, and c) reveal no relationship of aerobic fitness (within a moderate range) to right ventricular myocardial functional responses to an acute bout of progressive exercise. Within this model of acute exercise, then, no evidence was observed of unique right ventricular myocardial responses or fatigue. With increasing work loads right ventricular stroke volume was observed to initially rise by approximately 27 % in both groups and then remained essentially stable to maximal exercise. This pattern of “plateau” of stroke volume is identical to that consistently observed in assessment of left ventricular responses to progressive cycle exercise performed in the upright position
18
3.9
7.4 6.5 0.88
▶ Fig. 2–5). No significant differences were observed in these (● measures between the 2 groups, nor was any group × time interaction seen for any exercise variable (except for a minor interaction for E’).
15
Fig. 2 Tissue Doppler-S and E’ velocities, reflecting right ventricular systolic and diastolic function, respectively, during progressive exercise in aerobically-trained and untrained men. P > 0.05 for all group comparisons.
E / E’
Systolic function Peak pulmonary outflow velocity (cm s − 1) Rest 84 (11) 95 (15) Max 170 (17) 183 (12) Δ factor 2.02 1.93 Systolic ejection rate (ml s − 1) Rest 304 (39) 327 (51) Max 669 (110) 715 (98) Δ factor 2.20 2.19 TDI-S (cm s − 1) Rest 12 (3) 13 (3) Max 33 (8) 34 (5) Δ factor 2.8 2.6 Diastolic function Diastolic filling (E) (cm s − 1) Rest 51 (12) 49 (8) Max 121 (19) 135 (22) Δ factor 2.4 2.8 TDI-E’ (cm s − 1) Rest 16 (4) 15 (3) Max 42 (6) 49 (9) Δ factor 2.6 3.3 E/E’ Rest 3.26 (0.89) 3.31 (0.92) Max 2.88 (0.33) 2.87 (0.69) Δ factor 0.88 0.87
30
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 3 Right ventricular filling pressure estimated by E/E’ obtained by Doppler echocardiography during maximal progressive exercise in aerobically-trained and non-trained men. P > 0.05 for all group comparisons.
[21]. The initial increase has been attributed to mobilization of blood sequestered in the lower extremity when assuming the upright position. Other than this initial “refilling” phenomenon, then, stroke volume changes little during the course an acute bout of progressive exercise. Occurring concomitantly with a 3–4 fold rise in systemic venous return to the heart, this stability of stroke volume is explained by the rise in heart rate, which matches venous return and maintains a constant ventricular filling volume. It is evident, then, that the rise in ventricular inotropic and lusitropic function in such exercise serves to maintain stroke volume as the ejection time shortens.
Rowland T et al. Right Ventricular Responses to Exercise… Int J Sports Med 2014; 35: 987–993
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Non-trained
Previous
E’ (cm.s– 1)
Present study
40 S (cm.s– 1)
Table 1 Echocardiographic variables in the present study evaluating right ventricular function compared to previously published data assessing those of the left ventricle. Values are mean (standard deviation). No significant group or group-time interaction was observed except for group-time interaction for TDI-E’. *Left ventricular values are averages from multiple published sources in young, non-athletic subjects (see text for references).
200
POV (cm.s–1)
180 160 140 120 100 80 60
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 4 Peak pulmonary outflow velocities during progressive upright cycle in trained and non-trained men. P > 0.05 for all group comparisons.
840
Ejection rate (mL.s– 1)
740 640 540 440 340 240 140 40
0
3
6
9 12 Time (min)
Aerobically trained
15
18
21
Normally active
Fig. 5 Systolic ejection rate (stroke volume divided by systolic ejection time) during maximal exercise testing of aerobically-trained and nontrained men. P > 0.05 for all group comparisons.
The pattern of rise in the stroke volume in this study then indicates that a similar scenario occurs in the right ventricle. It also implies an appropriate augmentation of myocardial systolic and diastolic responses, since any dysfunctional response to this exercise model would be evidenced by a decline in stroke volume as work intensity increased [27]. Normal systolic and diastolic response to exercise in these subjects equivalent to those previously observed in the left ventricle is supported by the changes observed in other functional mark▶ Table 1. The values outlined in this table are ers outlined in ● compared to the average of resting and maximal values of previous reports assessing left ventricular function during upright or semi-supine cycle exercise to exhaustion in young nonathletic subjects. (References for average values for markers of left ventricular systolic function can be accessed in the review by Rowland and Unnithan [28], for mitral E [3, 24, 26, 29–31], and TDI-E’ [1, 9, 29–31]). Maximal-to-rest ratio for these variables in the present study ranged from 1.9 (systolic ejection rate) to 3.3 (TDI-E’), delta fac-
tors which are similar to or slightly greater than those previously described for left ventricular systolic and diastolic responses. However, certain specific absolute values at rest and during exercise are observed to vary from those reported for the left ventricle. Differences in longitudinal systolic (TDI-S) and diastolic (TDI-E’) values can be explained by the unique fiber orientation and contractile pattern of the right compared to the left ventricle [10]. Compared to the left ventricle, the right is a thin-walled (3–5 mm) crescent-shaped structure composed of 3 compartments, the inlet and apex (comprising the trabeculated sinus portion), and a smooth-walled outlet, or infundibulum. Contraction of the right ventricle starts inferiorly in the sinus and proceeds in a peristaltic motion towards the infundibulum, while the thick walled left ventricle contracts by a “wringing out” motion of helically-oriented, spiral fibers. In contrast to the left ventricle, too, the fibers of the right ventricular free wall are oriented primarily in a longitudinal direction, accounting for greater myocardial velocities with Doppler imaging. Lower peak velocities were recorded at rest and during exercise for diastolic tricuspid inflow (E) compared to previous experience with trans-mitral velocities. This mimics the findings of Zoghbi et al., who reported 22 % lower peak E velocities during tricuspid inflow compared to those at the mitral valve at rest [37]. E velocity reflects the gradient between upstream (right atrial) and downstream (right ventricular) pressure, which accounts for ventricular filling. During exercise, the former is dictated largely by heart rate (rising to match systemic venous return), while the latter is influenced by myocardial relaxation properties as well as ventricular post-systolic elastic recoil [21]. The normally-maintained stroke volume, expected max:rest E ratio and unchanged right ventricular filling pressure (as indicated by E/E’) imply that the balance of these 2 influences during exercise in this study was normal. Zoghbi et al. noted that a larger flow area of the tricuspid annulus compared to that of the mitral valve might be at least partly responsible for lower E velocities recorded in right ventricular inflow [37]. E/E’, an indicator of ventricular filling pressure, did not change significantly during the course of exercise, consistent with left ventricular studies that indicate a stable left ventricular end diastolic volume and close matching of rise in heart rate with augmented pulmonary venous return [24]. The pattern of E/E’ also mimicked that of previous left ventricular reports during upright exercise, with a small early rise as systemic venous return increases when blood is mobilized from dependent legs (Frank Starling effect), followed by a gradual decline to exercise exhaustion. The latter is consistent with a small but progressive decrease in left ventricular end diastolic dimension observed by echocardiography [20, 24]. In the present study, this can be presumed to reflect similar trends in right ventricular size during progressive exercise. No significant differences were observed in markers of systolic or diastolic function during exercise between the trained and non-trained subjects. This study thus provides evidence that within a moderate range of aerobic fitness, VO2max is independent of right ventricular myocardial functional responses to exercise. This finding is consistent with reports of left ventricular dynamics during the same exercise model [25, 30]. Instead, the primary factors which dictate individual variations in VO2max within the moderate range are those which influence ventricular diastolic size, including genetic pre-disposition, blood vol-
Rowland T et al. Right Ventricular Responses to Exercise … Int J Sports Med 2014; 35: 987–993
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Physiology & Biochemistry
ume, and resting bradycardia (by increasing ventricular filling time) [18]. Within the range of aerobic fitness included in this study, there is no evidence that either left or right ventricular inotropic or lusitropic functional responses to exercise contribute to individual variations in VO2max. La Gerche et al. supported this conclusion in a group of 55 subjects (comprised of 40 athletes and 15 non-athletes) whose mean VO2max was 51.4 ± 11.9 ml kg − 1 min − 1 with a range from 23.5 to 82.2 ml kg − 1min − 1 [7]. Semi-supine exercise was performed to an average heart rate of 177 bpm. Multivariate analysis revealed that tissue Doppler measures of systolic and diastolic function did not predict VO2max, which instead was related significantly only to resting right ventricular volume and left ventricular mass. Several limitations of this study should be noted. No direct comparisons of right ventricular functional responses to exercise were made with left ventricular responses. Test-retest reliability was not assessed. It was assumed that respiratory influences on right-sided flow velocities during exercise were minor. Findings were limited to young males within a limited range of aerobic fitness, and results cannot be assumed to reflect those in comparisons of subjects with low aerobic fitness and elite level endurance athletes.
Conclusions
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While the right ventricle may face a greater after-load during exercise than the left, no evidence was provided by this study of any perturbations from expected myocardial systolic or diastolic functional responses to an acute progressive exercise challenge. No differences were observed in right ventricular responses to progressive exercise between trained and untrained subjects, providing evidence suggesting that ventricular size rather than function is responsible for dictating level of aerobic fitness, at least within the moderate range of the study groups. This study supported the feasibility of utilizing standard Doppler echocardiographic techniques in examining right ventricular functional responses to exercise. With this method, future research can address the importance of such responses in both clinical assessment of patients with heart disease as well as the effects of high levels of training and competition in elite endurance athletes.
Acknowledgements
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The authors wish to express their gratitude to Prof. Patricia C. Fehling for her invaluable contributions to this study as well as to the enthusiastic subjects who volunteered to participate. Funding for this study was provided from the Student Opportunity Fund at Skidmore College.
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