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1Department of Health and Human Performance, Iowa State University, Ames, Iowa; and 2Department of Physical Education, Southern Illinois University, Carbondale, Illinois
Submitted 18 October 2004 ; accepted in final form 14 April 2005
| ABSTRACT |
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orthostatic tolerance; peripheral circulation; baroreceptor sensitivity
Much less attention has been given to the effects of exercise training on orthostatic tolerance in older adults. Aging has been associated with a higher incidence of orthostatic hypotension (21, 30), which might increase the risk of falls in this population. A greater predisposition to orthostatic hypotension as a result of endurance training in an older population would be undesirable. On the other hand, if endurance training improved blood pressure regulation, then it would further support the inclusion of this type of exercise training in current recommendations for fall prevention (18). In this regard, Fortney et al. (8) found that highly trained (52.4 ± 1.7 ml·kg1·min1) older participants had smaller decreases in cardiac volumes and mean arterial pressure (MAP) and smaller increases in heart rate (HR) in response to submaximal LBNP compared with a control group (31.0 ± 2.9 ml·kg1·min1). Tolerance per se was not assessed. In contrast, longitudinal studies of older individuals found cardiovascular responses to prolonged head-up tilt to be unchanged in the trained compared with the untrained participants (2, 12). However, Carroll and colleagues (2) specifically excluded participants who became presyncopal from their analysis, whereas only 10% of the individuals that Gabbett and colleagues (12) tested became presyncopal. Using a cross-sectional design and a protocol designed to evoke presyncope, we found that fit and unfit older individuals did not differ in their tolerance to maximal LBNP (16).
Cross-sectional studies suffer from the inability to differentiate between individuals who had low tolerance before training and those who became less tolerant as a consequence of training (6). Thus our cross-sectional study, while the first to assess the effects of chronic exercise training on orthostatic tolerance in older adults, was limited in its generalizability. To the best of our knowledge, no investigation to date has specifically assessed differences in tolerance to a maximal orthostatic challenge before and after an endurance-training program in older men and women. Furthermore, differences in the responses to submaximal LBNP stress between young and older fit and unfit groups suggested that, whereas the groups tolerated maximal LBNP equally well, they did so utilizing different mechanisms (16). The time course of the adaptations to exercise training, associated with these different mechanisms, may differ as well.
Calf venous compliance may be a critical factor in determining the cardiovascular stress associated with changes in orthostasis. Preventing fluid shifts into the legs markedly reduces reflex responses to an orthostatic stressor (15). Calf venous compliance may be lower in older adults (17, 19, 23), which some have suggested may help protect older participants during orthostatic stress (19, 38). Calf venous compliance is higher in endurance-trained young and older individuals (5, 10, 17, 22, 23). Tsutsui and colleagues (38) suggested that lower leg compliance was associated with higher orthostatic tolerance in old compared with the young participants. However, the generalizability of this observation is limited: since compliance was assessed during the LBNP protocol rather than during rest, 65% of the participants tolerated the orthostatic challenge, and fitness was not considered (38). Recent cross-sectional data suggest that endurance training may improve venous compliance without affecting tolerance to maximal LBNP (17). However, as with studies of the effects of exercise training on orthostatic tolerance, the extent to which preexisting differences in compliance affected these findings is unknown. Furthermore, the time course and mechanisms responsible for alterations in venous compliance are not completely understood. Determining the adaptation in venous compliance over 6 mo of endurance exercise training may provide insight into the mechanisms responsible for these changes.
In summary, it remains unclear whether chronic endurance training affects tolerance to an orthostatic challenge in older men and women in general and, more specifically, whether changes in venous compliance with endurance training may affect this tolerance. Therefore, the purposes of this investigation were to determine the effects of a 6-mo endurance-training program on calf venous compliance and the responses and tolerance to the orthostatic stressor of maximal LBNP in older men and women. We hypothesized that tolerance to maximal LBNP would decrease following the endurance-training protocol and that increased calf venous compliance would be associated with this reduced tolerance.
| METHODS |
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-blockade use (n = 4), various arrhythmias (n = 3), or significant cardiovascular disease discovered during the graded exercise test (n = 1). The 20 selected were free of overt cardiovascular disease and orthopedic limitations to exercise testing or training. They were randomly assigned to either an exercise or control group (exercise group: n = 10, 5 men, 5 women; control group: n = 10, 6 men, 4 women). Peak O2 uptake (
O2 peak) estimates were obtained for all of the participants using the time to termination of the stress test as the criterion (9). All of the women were postmenopausal, and none was on hormone replacement therapy during testing or intervention. Participant characteristics are summarized in Table 1.
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LBNP testing. Each participant reported to the laboratory no sooner than 48 h after the graded exercise test and, following instrumentation, was placed in a supine position inside the LBNP testing chamber. Once inside, they straddled a padded bicycle seat with their feet clear of the base of the chamber and sealed at the level of the iliac crest. Following 12-min rest at ambient barometric pressure, negative pressure was induced using a commercially available vacuum and quantified with a pressure transducer (PS309, Validyne, Northridge, CA). Graded LBNP was invoked with 10-mmHg increases in negative pressure every 4 min. The LBNP test was terminated when the participant completed 4 min at 100 mmHg, at the onset of presyncopal symptoms, or by participant request. Signs of impending presyncope included dizziness, nausea, profuse sweating, or a rapid change in blood pressure defined as either a decrease in systolic blood pressure by 25 mmHg or a decrease in diastolic blood pressure by 15 mmHg within 1 min. All participants refrained from any exercise, alcohol, tobacco, or caffeine ingestion for 12 h and food intake for 3 h before their LBNP test.
Assessment of cardiovascular responses.
Forearm blood flow (FBF) was measured by using mercury-in-Silastic strain gauge plethysmography (D.E. Hokanson, Bellevue, WA) (14) with the strain gauge placed around the proximal portion of the left forearm about one-third the distance from the olecranon to the ulnar styloid. A wrist cuff was used to occlude circulation to the hand during FBF measurements; FBF was assessed every 20 s. Blood pressure was measured every minute via a Dinamap (Johnson & Johnson Medical, Tampa, FL). HR was assessed continuously using five-lead electrocardiography. Stroke volume (SV) was determined every minute using impedance cardiography (Minnesota Impedance Cardiograph model 304B, Surcom, Minneapolis, MN) (31) and ensemble R-wave averaging on 55 s of data acquired in each 60-s period. The analog HR and FBF signals were input into an online personal computer system using commercially available software (BIOPAC, Santa Barbara, CA). The HR and impedance cardiograph signals were analyzed by using commercially available software (Microtronics Corp, Chapel Hill, NC) to determine SV and calculate cardiac output (
).
Venous compliance.
The test used was a modified version of that reported elsewhere (14, 23). Briefly, participants were placed in the supine position with the right leg elevated above heart level and supported at the ankle and thigh. Using the formula
r2 * L, where L is length, calf volume was calculated from four girth measures obtained equidistantly between the medial malleolus and the tibial plateau and one calf segment length. Changes in limb volume relative to baseline were measured noninvasively using strain gauge plethysmography at the maximal calf circumference. A venous-collecting cuff was placed
5 cm proximal to the knee on the right leg and inflated to 60 mmHg for 8 min and then reduced at a rate of 5 mmHg/5 s (over 1 min) to 0 mmHg.
Endurance-training protocol. The 6-mo aerobic training program consisted of the participants exercising 3 days/wk, 2045 min per session, at 4085% of HR reserve. The peak HR achieved during the stress test was considered the maximum HR. Resting HR was assessed weekly, and the target HR was adjusted biweekly. The duration and intensity of training were initially at the low end of these ranges due to the low initial fitness levels of the participants. It was increased accordingly such that, during the last 3 mo of the protocol, all participants were exercising at 6585% of their HR reserve for 40 min each session. Participants primarily trained their legs using treadmills and upright and recumbent cycle ergometers. The control group was instructed not to change their daily activity level. They were contacted every 2 wk to confirm their relative inactivity.
Within 2 wk of the participant's initial LBNP and calf venous compliance tests, all participants underwent the Senior Fitness Test Battery (29), which included a 6-min walk test for cardiovascular endurance. For the present study, this test was used as the measure of changes in cardiovascular fitness. This test was chosen to complement the results of the graded exercise test. In older unfit individuals, the limiting factor in a stress test is typically local leg fatigue or poor muscular endurance. Performance in the 6-min walk is another indicator of this local muscular endurance and more functionally practical.
Analysis.
LBNP tolerance was quantified as the LBNP tolerance index (LTI). This index was calculated as the sum of the products of duration spent at each negative pressure and the change in pressure from the previous stage (20). The LTI is a linear function for the conditions used in the present study.
was calculated every minute as the product of SV and the concurrent HR. MAP was determined every minute from the Dinamap. Forearm vascular conductance was calculated as FBF/MAP and total peripheral conductance (TPC) as
/MAP.
The anthropometric, estimated
O2 peak and LTI data were compared by using two-way repeated-measures ANOVA (group x trial). Mean cardiovascular responses for minutes 24 of each stage of LBNP common to all participants, the last completed stage of each participant, and each of the last 2 min of LBNP were compared by using three-way (group x trial x LBNP level) repeated-measures ANOVA for each variable. Post hoc comparisons were made by using the Tukey test. Statistical significance was set at 0.05, with data reported as means ± SE.
Determination of venous compliance entailed generating pressure-volume curves from the pressure-volume relationship as pressure was decreased at the rate of 5 mmHg/5 s from 60 to 10 mmHg. Pressure-volume curves were compared by means of the quadratic regression model [
limb volume =
0 +
1 * (cuff pressure) +
2 * (cuff pressure)2] for each individual, where
is change. Regression models were calculated using the general linear model procedure in SPSS and included between-participant classifications for age and training status. The pressure-volume relation is not linear; therefore, a single number is not sufficient to characterize the slope of the pressure-volume curve. Thus the group-averaged regression parameters
1 and
2, determined by the pressure-volume curves for each participant in the relevant groups, were used together as an estimate of compliance, such that compliance =
1 + 2 *
2 * (cuff pressure) or the derivative of the pressure-volume curve (14, 23). The coefficient of variation of this method has been reported to be 4.9% (23).
| RESULTS |
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O2 peak or 6-min walk performance preintervention, the exercise group performed significantly better on the 6-min walk test postintervention, whereas the control group did not change (14 ± 3 vs. <0.1 ± 2%; P < 0.05). None of the participants was a smoker, and none reported performing regular moderate or vigorous physical activity within the last year. None was overtly hypertensive, although four in the exercise group and three in the control group were prehypertensive. One participant in each of the exercise and control groups was moderately overweight (body mass index > 30 kg/m2). Average attendance at exercise sessions for all participants was 96%. Resting SV tended to be higher postintervention in the exercise group (P = 0.07), but there were no significant differences between groups or trials in the resting cardiovascular variables. Following the 6 mo of training, tolerance as expressed by LTI was not different either between groups or across trials (Table 1). Cardiovascular responses to submaximal LBNP. Hemodynamic responses to LBNP are illustrated in Figs. 13. Two participants became presyncopal (one woman and one man from the exercise group, initial trial) before 40 mmHg of LBNP and were excluded from the submaximal analyses. There were no significant main effect differences between the groups or trials. However, some LBNP x trial interactions were found.
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declined similarly (P < 0.05) (Fig. 2). There were no differences in MAP across the submaximal LBNP levels for either group, either before or after training. Forearm vascular conductance decreased below rest in the last completed stage in both groups only in the preintervention trial. The LBNP stage at which TPC decreased below rest in the exercise group was 20 mmHg preintervention and 30 mmHg postintervention (P < 0.05; Fig. 3), whereas TPC in the control group did not differ significantly from rest for either trial.
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was lower than rest for all groups in the last completed stage of LBNP, but it was lower than rest at 20 mmHg for the exercise group preintervention and at 30 mmHg postintervention (P < 0.05). MAP was significantly lower than rest at e-1 and the last minute of the test for only the preintervention trial in both groups (P < 0.05) (Fig. 2). Venous compliance. There were no differences in calf volume between groups either before or after the intervention (Table 1). There were no differences in either the slope of the pressure-volume relationship or the compliance between groups preintervention or after 3 mo of endurance training (P > 0.05). For brevity, the 3-mo data are not presented here. The slope of the pressure-volume curves tended to be greater postintervention in the exercise group (P = 0.08; Fig. 4, Table 2). Calf venous compliance was 2030% greater postintervention in the exercise group. No differences were found between trials in the control group (Fig. 4, Table 2).
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| DISCUSSION |
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Carroll and colleagues (2) found that a 26-wk endurance-training protocol did not alter cardiovascular responses to 70° head-up tilt in older men and women. Similarly, Gabbett and colleagues (12) found that a 12-wk cycling endurance-training program in healthy physically active older men elicited increases in
O2 peak (10%) without significant changes in cardiovascular responses to 90° head-up tilt. In neither study was orthostatic tolerance explicitly assessed (2, 12). Both in the present longitudinal study and in our cross-sectional work (16), we found small but statistically significant differences in the cardiovascular responses to submaximal LBNP. It is unclear if the disparate findings across these studies are due to differences in the individuals tested, the duration of the training programs, or the orthostatic challenge. Nevertheless, the relatively small differences pre- and posttraining that we have found, when coupled with the negative findings of these other studies (2, 12), suggests that improving fitness via endurance exercise training has little to no substantive influence on the cardiovascular responses to a submaximal orthostatic stress in an older population. On the other hand, the present investigation utilized a 6-mo endurance-training intervention that elicited a 14% improvement in fitness. Training, sufficient to increase fitness beyond that seen here, may have yielded different results (27). For example, Fortney and colleagues (8) tested very fit older individuals (52.4 ± 1.7 ml·kg1·min1) and saw differences in cardiovascular responses to submaximal LBNP compared with their less fit controls.
Carroll et al. (3) reported increased orthostatic tolerance in previously symptomatic older participants following 26 wk of combined endurance and resistance training that failed to alter maximum O2 uptake (
O2 max) significantly. In the present study, no differences in LTI were found between trials in the exercise group, suggesting that chronic endurance training does not alter tolerance to maximal LBNP in older men and women. However, the standard deviation and range of individual scores was lower after training (standard deviation: preintervention = 96 vs. postintervention = 70; range: preintervention = 369, postintervention = 260 mmHg/min; Fig. 6). In other words, the less tolerant participants generally became more tolerant after 6 mo of training, while the more tolerant participants did not change. This deserves further investigation since, as suggested elsewhere (4), it implies that endurance exercise training might improve orthostatic tolerance in less tolerant older individuals or, perhaps, those with symptomatic orthostatic hypotension.
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O2 peak of 45 ml·kg1·min1.
There might be gender differences in the responses of the cardiovascular system to endurance exercise training in older adults (34, 35). For example, women increase their
O2 max primarily by increasing oxygen extraction (34) without significant changes in left ventricular filling dynamics (35), whereas men predominantly increase
O2 max by improving left ventricular filling dynamics (35) and increasing SV (34). Regarding calf venous compliance, Monahan and Ray (24) found that young women and men differ in compliance both at rest and in response to baroreceptor unloading. However, in the present study, there were no gender differences found. Collectively, these two studies suggest that the gender difference seen in young adults (24) is removed with aging. Our findings also suggest that there is not a gender difference in the venous compliance responses to endurance training. However, the small sample sizes seen when gender is considered separately necessarily warrants caution when generalizing these results.
The effects of age and chronic exercise training on central arterial compliance (37) are reported to be very similar to the effects on calf venous compliance (17, 23). Compliance of both arteries and veins appears to decline with age and improve with chronic exercise (17, 23, 37). The mechanisms of change in compliance of both vessel types may be related to either alterations in the composition of the vessel wall, specifically the ratio of elastin to collagen, or to alterations in sympathetically mediated vascular tone. Aging is associated with a decrease in the elastin-to-collagen ratio in the venous wall (1) and is, therefore, the most likely contributor to decreasing compliance with age.
The mechanisms associated with adaptations to endurance exercise training are less clear. Tanaka and colleagues (37) found an increase in central arterial compliance in response to 13 wk of endurance training. They speculated that one potential functional determinant affecting compliance might be a reduction in sympathetic-adrenergic tone, either directly or by enhancing endothelial release of nitric oxide (37). While this mechanism is appealing, Halliwill and colleagues (14) demonstrated that sympathetic stimulation reduced unstressed venous volume without affecting venous compliance. These findings suggest that this is not a mechanism by which venous compliance is increased through endurance training (14). Therefore, it is most likely that venous vasculature compliance is increased by alterations in the composition of the vessel wall. These alterations would take time to occur, which may be why no changes in calf venous compliance were found after 3 mo of training in the present study but tended to be seen after 6 mo of training. Further research investigating the mechanisms responsible for increasing arterial and venous compliance with exercise training is warranted.
Several limitations exist with the present investigation. First,
O2 peak was estimated initially but American College of Sorts Medicine's 6-min walk test was used as the comparison measure of cardiovascular fitness pre- and postintervention. Given that performance on a graded exercise test is typically limited due to local leg fatigue (e.g., poor muscular endurance), we felt the 6-min walk test was functionally more appropriate. However, there were no differences in
O2 peak or 6-min walk performance between groups before training, yet training led to a 14% improvement in the latter. Improvements in the 6-min walk test should equate to improvements in cardiovascular fitness. In this context, the exercise group went from the 56th percentile in the 6-min walk test norms, which is what would be expected of a healthy older population, to the 84th percentile postintervention (29). It has been suggested that young participants with
O2 peak > 55 (27) or 65 ml·kg1·min1 (4) are prone to reduced orthostatic tolerance, although this finding is not universally seen (10). This suggests that there might be a threshold of fitness for deleterious effects of increasing fitness on blood pressure regulation in response to orthostatic stress. However, the association between chronic endurance training and orthostatic tolerance is certainly multifactorial. It is unknown if a fitness threshold exists for older adults and, if it does exist, what it is.
Second, while LBNP causes central hypovolemia, it is not literally an orthostatic stressor, since the participants remain in the supine position. Thus, while there is considerable overlap in the responses to head-up tilt, passive standing, and LBNP, this difference should be remembered when comparing the present results with studies using these other tools. Third, our participants were clinically healthy, and the results seen here may differ from those seen in less healthy older populations. Finally, the use of venous occlusion plethysmography to measure compliance is a measure of whole limb compliance that varies with age (14). This method assumes that venous-collecting cuff pressure is equal to venous pressure. The use of an 8-min collecting period should account for possible age-related differences in whole limb blood flow (14, 23).
In summary, to the best of our knowledge, this study is the first to utilize a longitudinal design to assess both orthostatic tolerance and calf venous compliance in older adults before and after an endurance exercise training program. The present investigation found that a 6-mo endurance-training program tended to improve venous compliance in older individuals and did so without compromising tolerance to maximal LBNP.
| FOOTNOTES |
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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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