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Medicine & Science in Sports & Exercise:
Basic Sciences: Original Investigations

Regulation of blood volume during training in post-menopausal women

STACHENFELD, NINA S.; MACK, GARY W.; DiPIETRO, LORETTA; MOROCCO, TAMARA S.; JOZSI, ALISON C.; NADEL, ETHAN R.

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The John B. Pierce Laboratory and Departments of Epidemiology & Public Health, and Cellular & Molecular Physiology, Yale University School of Medicine, New Haven, CT 06519

Submitted for publication June 1997.

Accepted for publication August 1997.

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Abstract

Abstract: In younger people the increase in aerobic capacity following training is related, in part, to blood volume (BV) expansion and the consequent improvement in maximal cardiac output. This training-induced hypervolemia is associated with a decrease in cardiopulmonary baroreflex (CPBR) control of peripheral vascular tone.

Purpose: To test the hypothesis that improvement in peak oxygen consumption(˙VO2peak) during training in older women is associated with specific central adaptations, such as BV expansion and a reduction in CPBR control of vascular tone.

Methods: Seventeen healthy older women were randomized into training (N = 9, 71 ± 2 yr) and control (N = 8, 73 ± 3 yr) groups. The training group exercised three to four times per wk for 30 min at 60% peak heart rate for 12 wk and then 40-50 min at 75% peak heart rate for 12 wk. The control group participated in yoga exercises over the same time period. We measured resting BV (Evans blue dye), ˙VO2peak, and the forearm vascular resistance response to unloading low pressure mechanoreceptors during low levels of lower body negative pressure (through -20 mm Hg) before and after aerobic training. The slope of the increase in forearm vascular resistance (response) per unit decrease in central venous pressure (stimulus) was used to assess CPBR responsiveness.

Results: Aerobic training increased ˙VO2peak 14.2% from 24.2 mL·kg-1·min-1 to 27.7 mL·kg-1·min-1 (P < 0.05), a smaller improvement than typically seen in younger subjects. Blood volume (59.9± 1.9 and 60.9 ± 1.9 mL·kg-1) and CPBR function(-3.98 ± 0.92 and -3.46 ± 0.94 units·mm-1 Hg) were similar before and after training.

Conclusions: These data indicate that the inability to induce adaptations in CPBR function may limit BV expansion during training in older women. In addition, the absence of these specific adaptations may contribute to the relatively poor improvements in ˙VO2peak in older women during short (10-12 wk) periods of training.

Blood volume expansion associated with aerobic exercise training has been demonstrated reliably in younger men(7,8,22) and in middle-aged and older female athletes 32. Training-induced hypervolemia contributes to the higher peak cardiac output during exercise and thereby improves peak oxygen consumption (˙VO2peak) (6). Specific mechanisms that contribute to an increase in intravascular volume after exercise have been recently identified. One such mechanism is attenuation of reflexes that detect small changes in central blood volume, the cardiopulmonary baroreflex (12). Gillen et al.(12) demonstrated an attenuation of the cardiopulmonary baroreflex control of peripheral vascular tone within 2 h of exercise, a time that precedes the blood volume expansion. Both short-term training studies(6,7,22) and comparisons of athletes and untrained individuals (3,21) support the hypothesis that cardiopulmonary baroreflexes are attenuated in physically active individuals. This physiological adaptation plays a permissive role in exercise-induced hypervolemia by allowing the additional volume to remain in the vascular compartment without eliciting a homeostatic response.

The role of cardiopulmonary baroreflex function in blood volume control is complicated by several factors associated with aging. For example, an age-associated decline in cardiopulmonary baroreflex function has been reported by Cleroux et al. (4). This decline may be related to alterations in cardiac structure and function, such as reduced vascular compliance (1,20,34). The age-associated changes in cardiopulmonary baroreflex function may restrict the ability to expand intravascular volume in older individuals and thereby limit improvements in ˙VO2peak during training. In recent studies aimed at exercise training in older people, only modest (10-15%) increases in˙VO2peak were reported(2,15,27), compared with those typically reported for young people (22-33%) with similar protocols(22,24). These modest improvements in˙VO2peak were associated with either no change(15) or very small increases in blood volume(2). Spina et al. (29,30) reported that training-induced increases in ˙VO2peak in older women are not generally accompanied by increases in cardiac output. One possible explanation for these latter findings is that blood volume expansion with exercise training is minimized in older subjects, particularly women. We propose that this inability to increase intravascular volume in older women is linked to the adaptability of the cardiopulmonary baroreflex. Therefore, the purpose of the present study was to determine whether 12 wk of moderate exercise training leads to an attenuation of cardiopulmonary baroreflex responsiveness and increased blood volume in women over 65 yr of age. We hypothesized that a modest increase in ˙VO2peak in older women would be achieved independent of reductions in cardiopulmonary baroreflex responsiveness and blood volume expansion.

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METHODS

Subjects. Seventeen healthy active older (>65 yr) women were recruited from a retirement community in Connecticut. The subjects were part of a larger program examining various physiological and metabolic responses to moderate endurance training. The women were randomly assigned to aerobic training (N = 9) or placebo control (N = 8) groups. Two women in the training group were unable to complete the training protocol because of illness; therefore, data from the seven remaining subjects in the training group were used in the analysis. These remaining seven subjects completed all exercise sessions. The subjects were free from cardiovascular and renal disease. No subjects were taking any medications. All subjects were given written clearance by their physician and completed a preparticipation ECG stress test. The subjects gave written informed consent to participate in the study, which had prior approval by the Human Investigation Committee of the Yale University School of Medicine.

Training protocol. The aerobic training group took part in a supervised program of treadmill (24 wk, N = 4) or trampoline (16 wk,N = 3) walking. Because we were interested in the effectiveness of moderate-intensity aerobic exercise, and not the efficacy of a specific exercise program, we offered a choice of two exercise modalities to encourage adherence to the training program. The use of differing exercise modes with a small range of both frequency (e.g., three to four sessions per week) and duration (9-12 months) of training has been demonstrated successfully by others (5,9,29,30). Initial training(“hardening”) consisted of treadmill/trampoline walking three times per week at 60% of peak heart rate as determined by an incremental exercise test for 20-30 min and was used to accommodate the subjects to the exercise modalities. During hardening, exercise intensity and duration were gradually increased to 40-50 min of training three to four times per week at 75% of peak heart rate. This protocol was then continued for the final 12 wk. Hardening lasted for 12 wk in the treadmill group and 4 wk in the trampoline group. All training sessions were supervised by the same technician. Subjects in the trampoline group walked on the treadmill for one session per week enabling us to monitor submaximal heart rate response to the training program.

The placebo control group participated in group stretching and yoga exercises (three to four times per week for 1 h session) designed specifically to provide a similar attention effect to that of the training group but to avoid an increase in aerobic capacity. Determinations of blood volume,˙VO2peak and response to lower body negative pressure were made on all subjects before hardening or beginning yoga, and after the training period.

Aerobic capacity. ˙VO2peak was measured during a treadmill test using a constant speed (2.0-3.5 mph), incremental grade (+2% every 2 min) protocol. We selected a walking speed that elicited 60-70% of their age-predicted maximal heart rate at 0% grade. ˙VO2 was determined from continuous recordings of O2 fraction (Applied Electrochemistry SA-3, Sunnyvale, CA), CO2 fraction (Beckman OM-11, Somerset, NJ) analyses of expired air and minute ventilation (Interface Associates, VMM-2, Laguna Niguel, CA). Subjects exercised until exhaustion and met at least two of three criteria for determining ˙VO2peak: respiratory exchange ratio > 1.1; plateau of the ˙VO2 with increased grade; or heart rate greater than age predicted maximal heart rate.

Plasma volume. On a separate day after a 12-h fast, resting plasma volume was determined by Evans blue dye (Macarthy Medical Co., Romford, Essex, UK) dilution with the subject supine for at least 60 min at 27°C. The procedure for blood volume measurements is described by Haskell et al.(16), with some modifications for our older subjects. A control blood sample was taken before the injection of 15 mg of Evans blue dye solution in 3 mL of saline through an indwelling venous catheter. Blood samples were taken from the catheter at 10, 20, and 30 min after the dye injection. Reported values are based on the peak absorbance reading, which was at the 10 min sampling time in all but one subject, in whom peak absorbance occurred at 20 min. Blood volume was calculated from the plasma volume using peripheral venous hematocrit measurements, corrected for trapped plasma (0.96) and peripheral sampling (0.91) (11,14).

Body composition. Percent body fat was measured with Bull calipers on the right side of the body to the nearest 0.5 mm. Skinfold measurements were taken at the triceps, supraileum, and anterior thigh, according to methods for estimating body fat in older women(25). Skinfolds were measured by the same trained technician on all subjects, before and after the exercise training program.

Cardiopulmonary baroreflex response. We assessed cardiopulmonary baroreflex control of forearm vascular resistance during a graded orthostatic challenge (lower body negative pressure, LBNP). On a day before the LBNP experiment, the subjects were familiarized with all testing procedures. On the day of the experiment, subjects were allowed a light breakfast and fluids(without caffeine) before 9:00 a.m. All measurements were made between 12:00 and 3:00 p.m. and were preceded by a 30-min quiet rest period during which time an 18 gauge intravenous catheter was placed in an antecubital vein of the left arm. The subjects lay supine, sealed at the iliac crest enclosed in the LBNP box with room temperature maintained at 27°C. Immediately before LBNP, a blood sample was taken for the measurement of total protein (TP), determined in triplicate by refractometry. The protocol involved a 4-min resting period, followed by 4 min each of 10° head down tilt (HDT), 0,-10, and -20 mm Hg. During the last 3 min of the control and subsequent periods, heart rate, arterial blood pressure, cardiac stroke volume, and forearm blood flow were measured.

Heart rate, determined from an electrocardiograph, was averaged over 25-s intervals. Beat-to-beat arterial blood pressure was measured from a middle finger using a Finapres blood pressure monitor (Finapres model 2300, Ohmeda, Louisville, CO). Cardiac stroke volume was measured noninvasively by impedance cardiography (Minnesota Impedance Cardiograph, Model 304B, Minneapolis, MN), with two silver tape electrodes placed around the neck and two around the torso. The distance between the inner tapes was made identical for pre- and post-training experiments. Cardiac stroke volume was calculated using the equation of Kubicek et al. (19) and was averaged(ensemble averaging) over 25 s.

We estimated central venous pressure during LBNP by the method of Gauer and Sieker (10). The subject lay in the lateral decubitus position with the left arm extended downward and relaxed. Peripheral venous pressure was measured continuously from a catheter in a large antecubital vein attached to a pressure transducer (Gould Statham P23 ID, Gould Instruments, Cleveland, OH) that was placed at the level of the mid-sternum. This method has been found to correlate well to directly measured central venous pressure(10,21). Measurements of central venous pressure were made in a separate session immediately before the supine LBNP experiment, using the same LBNP protocol except that a 3 min control period was followed by 2 min each of HDT, 0, -10, and -20 mm Hg LBNP.

Forearm blood flow was measured by venous occlusion plethysmography, using a mercury-in-silastic strain gauge placed around the right forearm(35). Blood flow to the hand was occluded with a wrist cuff inflated to > 250 mm Hg. The arm was relaxed and suspended slightly above heart level. Forearm vascular resistance was calculated as mean arterial blood pressure/forearm blood flow and expressed as mm Hg·mL-1·min-1·100 mL -1 tissue. Total peripheral vascular resistance was calculated by dividing mean arterial blood pressure by cardiac output and is expressed in mm Hg·min-1·L-1. The slope of the linear relationship between estimated central venous pressure and forearm vascular resistance during HDT through -20 mm Hg LBNP was used to derive cardiopulmonary baroreflex sensitivity. The intraclass correlation coefficient for test-retest reliability on the control group for forearm blood flow, central venous pressure, and the cardiopulmonary baroreflex slopes were r = 0.87, r = 0.86 and r = 0.91, respectively, indicating high reproducibility for these measured variables.

Statistics. Data are expressed as mean ± SEM. A repeated-measures ANOVA was used to assess within group differences before and after exercise training during the LBNP experiments in the training and control groups. For subject characteristics, ˙VO2peak, blood volume, cardiopulmonary baroreflex slope, and cardiovascular parameters during the LBNP tests, we used a 2 × 2 ANOVA to determine differences between groups, and any group by time interactions. Based on an alpha level of 0.05 and a sample size of 7, our beta level (power) was ≥ 0.80 for detecting effect sizes of 1.9 units·mm-1 Hg and 7.5% (≈380 mL) for the gain of the cardiopulmonary baroreflex slope and blood volume(22), respectively. Data were analyzed using BMDP statistical software (BMDP Statistical Software Inc., Los Angeles, CA).

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RESULTS

Pretraining ˙VO2peak, blood volume and plasma protein concentration were similar between groups (Table 1), as were pretraining cardiovascular parameters (Table 2). Mean arterial pressure was similar pre- and post-training in both groups (96± 4 and 96 ± 4 mm Hg, for training and control groups, respectively), and although baseline FBF was slightly lower in the control group, this difference was not significant. Endurance training increased˙VO2peak by 3.5 ± 0.5 mL·kg-1·min-1 (14.2%) in the training group, with no changes in blood volume, plasma volume, plasma proteins, or body weight(Table 1). Neither ˙VO2peak nor body weight changed in the control group. Blood volume and plasma volume decreased (6.2% and 4.2%, respectively, P < 0.05). There was a decline in resting stroke volume in the control group only over the training period (group by time, P < 0.05), but no change in any cardiovascular variable in the training group.

Table 1
Table 1
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Table 2
Table 2
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Cardiopulmonary baroreflex function. The cardiovascular responses to LBNP were proportional to the orthostatic stress in both groups(Table 3). Mean arterial pressure did not change in either group during application of low levels of LBNP, averaging 96 ± 4 mm Hg (Table 3). The decline in estimated central venous pressure was also similar for the training and control groups before (-5.7± 0.8 and -5.3 ± 0.8 mm Hg) and after (-6.3 ± 1.7 and-4.1 ± 0.6 mm Hg) training. The decline in stroke volume was proportional to the decline in central venous pressure in both groups and was unaffected by training (Fig. 1). Reflex forearm vasoconstriction occurred at all levels of LBNP in response to the reduction in central venous pressure in both groups (Table 3), but the slope of the linear relationship between forearm vascular resistance and estimated central venous pressure were similar for the training (-3.98± 0.92) and control (-3.46 ± 0.96 units·mm-1 Hg) groups. Exercise training had no effect on the slopes of the forearm vascular resistance-central venous pressure, which averaged -3.46 ± 0.94 and-2.88 ± 0.90 units·mm-1 Hg for training and control groups, respectively (Table 1, Fig. 2).

Table 3
Table 3
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DISCUSSION

Older women generated only a modest improvement in ˙VO2peak (3.5 mL·kg-1·min-1) after endurance training (75% of peak heart rate). The significant new finding of this study is that the increased ˙VO2peak was not accompanied by an increase in blood volume or a reduction in cardiopulmonary baroreflex sensitivity. The absence of these characteristic central adaptations associated with endurance training in young people suggests a limitation in older women to increase˙VO2peak after a training stimulus.

Exercise training of similar and even lesser intensity and duration in young subjects leads to substantially greater increases in ˙VO2peak(≈22-33%) than we observed in older women(22,24). In addition, the increase in˙VO2peak is accompanied by an increase in blood volume(22) and the attenuation of peripheral vascular responses to cardiopulmonary baroreceptor unloading(22). Attenuation of cardiopulmonary baroreflex sensitivity may well be an important precursor to exercise-induced blood volume expansion in young men (12) because it permits a greater retained volume at any given cardiac preload (8). However, this adaptation did not occur in our older women volunteers and may explain, in part, the absence of a training-induced blood volume expansion. The stimulus-response characteristics of the cardiopulmonary baroreflex may be influenced by the reduced vascular compliance accompanying aging(1,34) and thereby limit the adaptability of this reflex. For example, the impairment of the cardiopulmonary baroreflex control of forearm vascular resistance in hypertensives is more pronounced in patients with left ventricular hypertrophy (13). It is likely that the reduced myocardial (20) or vascular compliance(1,34) that accompany normal aging limit central cardiovascular adaptations to endurance training in older people.

Cardiopulmonary baroreflex function may be protected during exercise training in older people because of an already reduced low pressure baroreceptor sensitivity. Cleroux et al. (4) demonstrated a reduced cardiopulmonary baroreflex response in older men versus younger controls, and we observed an age-associated reduction in volume receptor sensitivity to central volume expansion (31). Recent data have demonstrated intact discreet cardiopulmonary and carotid baroreceptor function in older people (28,33). However, Shi et al. (28) showed that the interaction of these two populations of receptors was absent in older people. Therefore, even if low-pressure baroreceptor function is unaffected by age, the lack of central integration of receptors with afferents indicates some impairment of blood pressure and/or volume regulation.

The reduction in cardiopulmonary baroreflex function after exercise training is part of a complex adjustment that leads to blood volume expansion. In young people exercise is a also strong stimulus for increasing circulating proteins, which increase oncotic pressure and favor fluid movement into the vascular compartment (7,11). Recent data from our laboratory have demonstrated a negative correlation between transcapillary escape rate of albumin and plasma volume expansion after intense exercise in young people (16). However, the level of total circulating protein was unaffected by training in our older subjects, and there is no evidence that intravascular protein increases after exercise in older people. In addition to increasing total proteins, increases in fluid intake and retention are also important components to the overall body water expansion that occurs after exercise training (6). Recent studies have demonstrated delayed or inadequate rehydration following exercise in older people (23,36), suggesting other components, such as thirst and fluid retention, of the hypervolemic response may also be absent in older people.

The lack of central cardiovascular adaptation after training suggests that the primary adaptations to training in older women occur in the periphery. Indeed, there is evidence in older women that exercise training augments peak arteriovenous O2 difference (29,30), increases skeletal muscle capillarization, fiber size, and distribution, and alters glycolytic and mitochondrial enzyme activities(5), without significant improvements in left ventricular function (26), maximal stroke volume, or cardiac volume(29,30). In the absence of these central cardiovascular adaptations with training, older women can increase˙VO2peak without blood volume expansion and the consequent increases in maximal cardiac output, although the increase in˙VO2peak is limited.

The modest increases in ˙VO2peak in the present study cannot be attributed to an inadequate exercise intensity. We set training intensity at a relative intensity similar to that used by younger subjects(22). In studies on older men employing either a more a rigorous training intensity (24) or a longer duration(9-12 months) (17,18,27,29), increases in ˙VO2max were similar to those of younger subjects. While none of these studies measured blood volume, the older women in the training study of Spina et al. (29) failed to increase maximal cardiac output even with their more rigorous training protocol.

In summary, we found that endurance training for 12 wk in older women induced only a modest increase in ˙VO2peak, which was not associated with an alteration in blood volume or cardiopulmonary baroreflex sensitivity. These findings are consistent with other investigations of older people (2,15) and with the hypothesis that improved oxygen transport capacity is caused by peripheral vascular or cellular mechanisms rather than central cardiovascular adaptations in older women (5,29). The inability to induce adaptations in cardiopulmonary baroreflex function likely contributes to the inability to increase blood volume, providing evidence for the role of these adaptations in blood volume expansion.

We gratefully acknowledge the technical support of Cheryl Weseman-Kokoszka and John R. Stofan and the cooperation of the volunteer subjects. This work was supported in part by NIH grant AG 09872.

Address for correspondence: Nina S. Stachenfeld, The John B. Pierce Laboratory, 290 Congress Avenue, New Haven, CT 06519. E-mail:nstach@jbpierce.com.

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Keywords:

AGING; EXERCISE; CARDIOVASCULAR FUNCTION; BLOOD PRESSURE; CARDIOPULMONARY BAROREFLEX FUNCTION; LOWER BODY NEGATIVE PRESSURE

©1998The American College of Sports Medicine

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