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Diastolic ventricular interactions in endurance-trained athletes during orthostatic stress

¹Cardiovascular Physiology and Rehabilitation Laboratory, University of British Columbia, Vancouver, British Columbia; ²Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, Alberta; and ³Division of Sports Medicine, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada

Submitted 26 August 2006 ; accepted in final form 10 March 2007

	ABSTRACT

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Enhanced left-ventricular (LV) compliance is a common adaptation to endurance training. This adaptation may have differential effects under conditions of altered venous return. The purpose of this investigation was to assess the effect of cardiac (un)loading on right ventricular (RV) cavity dimensions and LV volumes in endurance-trained athletes and normally active males. Eight endurance-trained (VO_2max, 65.4 ± 5.7 ml·kg^–1·min^–1) and eight normally active (VO_2max, 45.1 ± 6.0 ml·kg^–1·min^–1) males underwent assessments of the following: 1) VO_2max, 2) orthostatic tolerance, and 3) cardiac responses to lower-body positive (0–60 mmHg) and negative (0 to –80 mmHg) pressures with echocardiography. In response to negative pressures, echocardiographic analysis revealed a similar decrease in RV end-diastolic cavity area in both groups (e.g., at –80 mmHg: normals, 21.4%; athletes, 20.8%) but a greater decrease in LV end-diastolic volume in endurance-trained athletes (e.g., at –80 mmHg: normals, 32.3%; athletes, 44.4%; P < 0.05). Endurance-trained athletes also had significantly greater decreases in LV stroke volume during lower-body negative pressure. During positive pressures, endurance-trained athletes showed larger increases in LV end-diastolic volume (e.g., at +60 mmHg; normals, 14.1%; athletes, 26.8%) and LV stroke volume, despite similar responses in RV end-diastolic cavity area (e.g., at +60 mmHg: normals, 18.2%; athletes, 24.2%; P < 0.05). This investigation revealed that in response to cardiac (un)loading similar changes in RV cavity area occur in endurance-trained and normally active individuals despite a differential response in the left ventricle. These differences may be the result of alterations in RV influence on the left ventricle and/or intrinsic ventricular compliance.

diastole; left ventricular compliance; right ventricle

Although increased LV compliance may be beneficial during exercise, this adaptation may be detrimental under certain conditions. It is well established that endurance-trained athletes have a decreased tolerance to orthostatic stress compared with sedentary or normally active individuals (14, 24, 25). Because a given drop in LV filling pressure results in a larger reduction in LVEDV for athletes, it has been proposed that the enhanced LV compliance of endurance-trained individuals may contribute to their relative orthostatic intolerance (15). The influence of RV filling on LV compliance may play an important role during reductions in venous return (20). In fact, it has been postulated that endurance-trained athletes may lack the diastolic ventricular interaction necessary to compensate for sudden reductions in RV volume, making them more prone to orthostatic hypotension (12). This hypothesis is supported by animal literature (12) but has not been previously tested in endurance-trained humans.

The purpose of this investigation was to assess the effect of cardiac (un)loading on RV cavity dimensions and LV volumes in endurance-trained athletes and normally active males. We hypothesized that in response to altered venous return, endurance-trained individuals would exhibit greater changes in LVEDV and LVSV, despite similar changes in RV cavity area, compared with normally active individuals.

	METHODS

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Participants

We recruited eight healthy, normally active males who were not participating in a regimented exercise program (VO_2max < 50 ml·kg^–1·min^–1) and eight endurance-trained males who trained in excess of 10 h/wk and were competitively active for at least the past three years (VO_2max > 60 ml·kg^–1·min^–1). Each individual underwent 3 days of testing with at least 2 days between data-collection sessions.

This investigation was approved by the Clinical Research Ethics Board of the University of British Columbia, and informed consent was provided by all participants before testing. All testing was conducted in accordance with the Declaration of Helsinki.

Experimental Day 1: Familiarization and Assessment of VO_2max

Each participant underwent an incremental, staged exercise test on an electronically braked cycle ergometer (Ergometrics er800s; Ergoline, Bitz, Germany) to assess VO_2max. Expired gases were collected and analyzed with a metabolic cart (MAX-I Mark B; Physiodyne, Quogue, NY). Following the exercise test, participants were familiarized with the lower-body pressure chamber used on days 2 and 3 of the investigation.

Experimental Day 2: Assessment of Orthostatic Tolerance

The purpose of experimental day 2 was to determine if there was a greater incidence of presyncopal episodes during an orthostatic challenge among the endurance-trained athletes. The testing session began with 15 min of supine rest before the orthostatic tolerance test. Participants remained supine throughout the pressure challenge and were sealed in a lower-body pressure chamber at the level of the iliac crest. The orthostatic challenge began at 0 mmHg (atmospheric pressure) and progressed by increments of –20 mmHg up to a maximum of –80 mmHg. Each pressure stage lasted 5 min. Presyncope was determined by a sudden drop in heart rate or blood pressure or a sustained decrease in systolic blood pressure below 90 mmHg. Qualitative symptoms such as nausea, dizziness, profuse sweating, and/or light headedness were also used to signify presyncope. Cardiac output was measured by using the single breath-hold technique (using acetylene as the soluble gas; Medisoft Ergocard, Dinant, Belgium) in the final minute of each stage (30). Heart rate (electrocardiogram) and blood pressure (automated sphygmomanometer; VSM MedTech, Vancouver, BC, Canada) were also continuously monitored during the tolerance test.

Experimental Day 3: Lower-Body Negative and Positive Pressure with Echocardiography

Pressure challenges. The third day of testing involved 15 min of supine rest followed by both a lower-body negative pressure (LBNP) and lower-body positive pressure (LBPP) challenge (randomly assigned). The LBNP challenge began at 0 mmHg and decreased to –20 mmHg for 3 min. Participants were then returned to 0 mmHg for 3 min or until heart rate and blood pressure returned to resting values (whichever was longer). The pressure was then decreased to –40 mmHg for 3 min. This protocol was repeated for –60 and –80 mmHg. The same protocol was used during LBPP with pressures of 20, 40, and 60 mmHg above atmospheric pressure. Ten minutes of supine rest were given (or until heart rate and blood pressure returned to resting values) between the LBPP and LBNP challenges. Heart rate and blood pressure were monitored throughout the pressure challenges.

Echocardiogram acquisition. Participants lay in the pressure chamber in a slight left lateral decubitus position. A Sonos 5500 (Philips) was used to acquire two-dimensional and Doppler echocardiogram recordings at rest and at each stage of the lower-body pressure challenge. All echocardiographic imaging was conducted by a single, experienced clinical sonographer and was completed in accordance with American Society of Echocardiography guidelines (27). At rest, baseline recordings of Doppler peak flow velocities (mitral, tricuspid, and pulmonary venous flow) and a minimum of four cardiac cycles in the long-axis view were acquired. LV mass (7) was also calculated. The apical four-chamber view was obtained immediately before each pressure challenge (for at least four cardiac cycles) and immediately following the onset of lower-body pressures (for 10 cardiac cycles) to provide simultaneous indices of RV and LV dimensions. We measured RV and LV septal-to-free-wall diameter and cavity area in diastole as well as LV end-systolic cavity area. LV volumes were calculated by using the single-plane method of discs (27). Pulse wave Doppler recordings of mitral, tricuspid, and pulmonary venous flow were made between 30 s and 1 min from the start of each pressure stage. From the Doppler recordings, peak flow velocities of early and atrial filling were measured. Peak systolic, diastolic, and reverse flows were measured from the right pulmonary vein. By using the duration of the mitral a-wave (MA) and pulmonary venous reverse flows (PVRF), LV end-diastolic pressure was estimated [LVEDP = 16.8 + 0.117 x (PVRF-MA)] (18, 26). Lastly, the sonographer returned to the apical four-chamber view to record four additional cardiac cycles in a "steady-state" situation (at min 3 of the pressure challenge). All echocardiography data were recorded on a high-quality VHS tape and were analyzed by a single trained observer who was blinded to the group and pressure stage during measurement.

Data Analysis

For all stages, apical four-chamber results were analyzed at rest (the average of at least four cardiac cycles before the onset of pressure), during 10 cardiac cycles immediately following the onset of pressure (beat-by-beat measures), and at min 3 of each pressure challenge (average of four cardiac cycles). The Doppler recordings are an average of at least four cardiac cycles before the start of the first pressure (original rest) and at min 1 during each pressure stage.

Pressure-volume curves were generated for each individual based on their LVEDV and estimated LVEDP at rest and at min 3 of each pressure stage. The slope k was determined for each individual by using the equation P = ae^kV + b, where P is pressure, V is volume, and a, e, and b are constants (15, 19). Group means and standard deviations for k were calculated and compared. LV stiffness is equivalent to k; therefore, compliance is equivalent to 1/k (15).

Statistics

A three-way mixed-model ANOVA was run by using STATISTICA 6.0 software (StatSoft) to compare differences between groups, between pressures, and at various times following the onset of pressure with Tukey post hoc comparisons. An independent t-test was used to establish group differences for physical characteristics as well as LV stiffness and compliance. The level of significance was set a priori at P < 0.05.

	RESULTS

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Participant Physical Characteristics

Normally active and endurance-trained participants did not differ in height, mass, or age (Table 1). By design, the endurance-trained athletes had significantly higher relative and absolute VO_2max values and exercised aerobically for more hours per week (Table 1; P < 0.05). LV mass (306.0 ± 68.0 vs. 251.2 ± 77.8 g), resting LVEDV (112.0 ± 18.0 vs. 94.9 ± 25.4 ml), LVSV (78.0 ± 16.6 vs. 65.0 ± 15.5 ml), and RV end-diastolic cavity area (18.6 ± 3.9 vs. 16.6 ± 3.1 cm²) were all higher in the endurance-trained group but not significantly different. Heart rates were also greater at rest in the normally active individuals (65 ± 15 vs. 54 ± 8 bpm), but these differences were not statistically significant. There were no statistical differences in systolic (118 ± 10 vs. 120 ± 6 mmHg), diastolic (63 ± 6 vs. 63 ± 8 mmHg), or mean (81 ± 7 vs. 82 ± 7 mmHg) arterial blood pressures at rest between the normally active and endurance-trained groups.

Seven out of eight endurance-trained individuals did not complete the orthostatic tolerance test on experimental day 2. The tests were stopped due to falling arterial blood pressure (four athletes had decrease in systolic blood pressure below 90 mmHg) and/or light headedness (three athletes reported feeling extremely light headed). All eight normally active individuals completed the orthostatic challenge without signs of presyncope. Because the majority of the endurance-trained individuals did not complete the final pressure stage, statistical comparisons were only made from rest through to –60 mmHg. Heart rate progressively increased during the orthostatic challenge to the same extent in both groups. LVSV decreased in both groups; however, it decreased to a greater degree in the endurance-trained athletes (P < 0.05). Cardiac output was reduced in both groups but to a greater extent in the endurance-trained group (P < 0.05).

Ventricular Dimensions

RV end-diastolic cavity area was reduced during LBNP and increased during LBPP from rest to the same degree in both the normally active and endurance-trained groups (Fig. 1). There was also no difference between groups in the response of RV end-diastolic septal-to-free-wall diameter during LBNP or LBPP. Overall, the right ventricle responded to cardiac loading and unloading in the same manner for both groups (Table 2).

View larger version (12K): [in this window] [in a new window]   Fig. 1. Right ventricular (RV) end-diastolic cavity area during cardiac loading and unloading. RV end-diastolic cavity area during lower-body negative (LBNP; A) and positive pressure (LBPP; B) in the normally active group (solid line) and endurance-trained group (dashed line) are shown. Representative data are shown at –80 and +60 mmHg. Beat 0 refers to the resting average, beats 1–10 are immediately following the onset of pressure, and beat 11 is the 3-min average. Values are presented as group means ± SE.

View larger version (12K): [in this window] [in a new window]   Fig. 2. Left-ventricular end-diastolic volume (LVEDV) during cardiac loading and unloading. LVEDV during LBNP (A) and LBPP (B) in the normally active group (solid line) and endurance-trained group (dashed line) are shown. Representative data are shown at –80 and +60 mmHg. There was a statistically significant interaction effect (pressure x beat x group; *P < 0.05). Beat 0 is the resting average, beats 1–10 are immediately following the onset of pressure, and beat 11 is the 3-min average. Values are presented as group means ± SE.

View larger version (12K): [in this window] [in a new window]   Fig. 3. Left ventricular end-diastolic pressure (LVEDP)-LVEDV relationship. The slope of the pressure-volume relationship for the normally active individuals was significantly greater than for the endurance-trained group (*P < 0.05). Data include rest (before any pressure challenges), 3 positive pressures (above rest, at steady state), and 4 negative pressures (below rest, at steady state). Values are presented as group means ± SE.

LVSV of endurance-trained individuals was more sensitive to the pressure changes, resulting in greater decreases in LVSV during LBNP and larger increases during LBPP compared with normally active individuals (P < 0.05) (Table 2). Group mean heart rates were consistently, but not statistically, higher in normally active individuals at rest and throughout the pressure challenges. There were no statistical differences in the way in which the groups’ heart rates responded to the pressure challenges (Table 3). Cardiac output responded to the pressures as expected, with the highest output coming from the highest positive pressures and vice versa. Largely owing to the differences in LVSV, there were also differences in the response of cardiac output between groups (Table 3; P < 0.05).

Both systolic and diastolic pulmonary venous flow velocities were significantly decreased with LBNP and increased with LBPP; however, there were no differences in the way the groups responded. Peak pulmonary reverse flow velocity increased incrementally with the application of LBNP and decreased with LBPP; however, the groups did not respond differently (Tables 4 and 5).

	DISCUSSION

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The major new finding of this investigation is that despite a differential LV response to altered cardiac (un)loading, there is a similar change in RV cavity area in both groups. We also found that in response to cardiac (un)loading, the normally active individuals showed a greater change in estimated LVEDP, whereas endurance-trained athletes had larger changes in LVEDV. Altered LV compliance in endurance-trained athletes has been shown previously (15) but not in conjunction with measures of RV dimensions.

We propose that RV filling was affected primarily by altered venous return similarly in both groups, whereas the left ventricle appears to have been affected by external constraints in addition to alterations in filling pressure (5, 20, 21). These external pressures acting on the left ventricle may include pericardial tension and interaction with the right ventricle (5). This may partially explain the divergent responses between the groups on the left but not the right side of the heart.

During the interpretation of our results, we have made the assumption that a relatively large change in estimated LVEDP in the normally active males, despite small volume changes, is indicative of external constraints acting on the left ventricle. It is likely that other factors such as the intrinsic properties of the myocardium also contribute to the differential LV response seen in this investigation; however, the majority of this discussion focuses on the potential of ventricular interaction because we measured ventricular dimensions and not intrinsic myocardial properties. Indeed, it has been shown that 30–40% of resting LV pressure is created by external forces that are independent of LV volume (5). Our results, and those of others (15), show that at rest normally active individuals have a higher estimated LVEDP and a lower LVEDV (Fig. 3). The higher pressure may be a result of greater external constraints on the left ventricle.

Responses to LBNP

Diastolic ventricular interactions may play a significant role in explaining the ability of the normally active individuals to maintain their LV volumes to a greater extent despite a similar reduction in RV cavity area. With LBNP, RV cavity area (and likely external constraint to the left ventricle) was reduced. The partial removal of external constraints on the left ventricle could lower LV pressure, causing an increased LV filling gradient (20). The filling gradient was not increased in either group, although LV filling was maintained to a greater extent in the normally active individuals in the face of reduced venous return (4, 10).

Minimum LV pressure is reduced following reductions in RV volume, allowing for an increase or maintenance of the transmitral filling gradient despite reduced venous return (17). Two separate investigations have shown that decreasing RV preload leads to a downward shift in the LV diastolic pressure-volume relationship, allowing for greater LV filling at a given pressure (1, 17). These findings are similar to what may have occurred in the normally active individuals during LBNP. In patients with heart failure, Atherton et al. (3) found that with reductions in RV volume, LVEDV was paradoxically increased. This finding was attributed to increased LV compliance due to the reduction of external constraints, namely the pericardium and right ventricle, on the left ventricle (3).

The Doppler peak flow velocities obtained during LBNP are consistent with the ventricular dimension data. Early mitral peak flow velocity was maintained to a greater extent in the normally active individuals, supporting the notion that their LV filling gradient was maintained to a greater extent (4, 10). This divergent response was seen despite similar reductions in early tricuspid peak velocities and pulmonary venous systolic and diastolic peak velocities in both groups.

Responses to LBPP

During LBPP, RV cavity area increased to the same extent in both groups; however, LVEDV was increased to a greater degree in endurance-trained individuals. In the normally active group, we propose that as RV cavity area increased, the amount of external constraint on the left ventricle increased as well (5). This is evident by the large increases in estimated LVEDP during LBPP in the normally active individuals in this study and in others (15). Increased RV cavity area could increase external pressure on the left ventricle in two ways: 1) by increasing total cardiac volume and therefore pericardial pressure, and 2) by shifting the interventricular septum toward the left ventricle, making the left ventricle temporarily less compliant (20, 22). We propose that the left ventricle of endurance-trained individuals has less external constraint acting on it compared with the left ventricle of normally active individuals, resulting in a greater ability to increase LVEDV when RV cavity area is increased. Again, the findings of changes in LVEDV and RV cavity areas are supported by the Doppler flow velocities and estimated LVEDP.

Ventricular Compliance and the Pericardium

Chronically trained endurance-trained athletes may provide a case in which pericardial, and therefore LV, compliance can be altered. Research in dogs has suggested that a chronic increase in ventricular filling can stimulate pericardial growth (8, 16). Following 9 wk of elevated right-atrial preload (as a result of an arteriovenous fistula), the pericardium increased in both size and mass (8). Interestingly, the diastolic pressure-volume curves of normally active individuals and endurance-trained athletes developed in the present experiment [as well as those of Levine et al. (15)] are similar to the diastolic pressure-volume relationships of the normal canine heart and the canine heart following chronic volume loading, respectively (8, 15). The necessary stimulus may be present in endurance-trained athletes to provoke pericardial and myocardial remodeling in the form of exercise-induced hypervolemia and years of exercising at high LVEDV (28, 29).

If pericardial and/or myocardial remodeling has occurred, this could potentially reduce diastolic ventricular interaction in response to acute changes in venous return. An increased LV compliance as a result of reduced influence of the right ventricle on LV filling may be beneficial when ventricular volumes are increased but detrimental during reductions in venous return.

It should be noted that any discussion of the pericardium as a contributing factor to the results of this investigation are purely speculative. Animal literature suggests the pericardium has an important influence on ventricular interaction (12). However, the effects of the pericardium on this investigation were not quantified.

Limitations. Echocardiography provides a two-dimensional image of a three-dimensional organ, yet LV volumes were calculated by using well-standardized and validated equations. It is also technically difficult to acquire clear images of the right ventricle; however, meticulous care was taken to provide clear images of both sides of the heart. Our measurements of RV area are consistent with others currently in the literature (6, 23), and the findings on both sides of the heart are congruent with the Doppler indices, which are less sensitive to the position of the right ventricle. Moreover, the methods were applied consistently and reliably across groups, allowing justifiable comparisons.

All of the measures made in this study were noninvasive, and therefore we cannot identify true cardiac or pericardial pressures. However, we feel that the results of previous invasive investigations provide strong empirical support for our noninvasive findings.

Conclusion

Our findings indicate that the more compliant left ventricle seen in endurance-trained individuals may partially be due to reduced influences of the right ventricle. The resultant differences in compliance between endurance-trained and normally active individuals may be functionally significant when venous return is altered during conditions such as exercise or an orthostatic challenge.

	GRANTS

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B. T. A. Esch and J. M. Scott were funded by the Natural Sciences and Engineering Research Council of Canada, the Canadian Space Agency, and the Michael Smith Foundation for Health Research during this project. This research project was funded by the Canadian Foundation for Innovation, the BC Knowledge Development Fund, and the Natural Sciences and Engineering Research Council of Canada. D. E. R. Warburton is supported by a Michael Smith Foundation for Health Research Scholar Award and a Canadian Institutes of Health Research New Investigator Award. M. J. Haykowsky was supported by a Canadian Institutes of Health Research New Investigator Award.

	ACKNOWLEDGMENTS

 
We thank the participants for their time and interest. We are also indebted to the enthusiastic service of Lan Hu.

	FOOTNOTES

 

Address for reprint requests and other correspondence: D. E. R. Warburton, Cardiovascular Physiology and Rehabilitation Laboratory, Univ. of British Columbia, 6108 Thunderbird Blvd., Vancouver, BC V6T 1Z3, Canada (e-mail: darren.warburton{at}ubc.ca)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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