Forced vital capacity (FVC) is decreased by as much as 0.5 L after exercise of varying durations and intensities (4,17,23). Among the factors that have been implicated in this reduction in FVC and other spirometric changes are respiratory muscle fatigue, pulmonary edema, exercise-induced bronchoconstriction, and increased thoracic blood volume (4,7,12,16,18,22). Since exercise increases pulmonary blood volume, it is suspected that this blood volume shift may be one of the causes of the decreased vital capacity seen following exercise. Stated simply, an increased volume of blood in the thorax may displace air and decrease spirometric volumes. Therefore, the purpose of this study was to examine the effects of changes in thoracic blood volume, independent of exercise, on several measures of lung function.
Previous studies that examined the effect of altered thoracic blood volume on various cardiovascular and respiratory measurements were often interested in simulating space flight and its consequent weightlessness, bed rest, or other physiological conditions besides exercise. To do this, they generally used either water immersion (5,25,26) or postural changes (8,17,21) to accomplish the blood volume shift, or bed rest to decrease blood volume (2). These perturbations, however, also create external loads on the chest wall, in the case of water immersion, or displace abdominal contents into the thoracic cavity in all cases. They would not, therefore, be applicable to the exercise situation, in which blood volume is shifted toward the thorax without displacing the abdominal contents or creating an extra load on the chest wall. Therefore, it was the more specific purpose of this study to examine the effects of lower body negative or positive pressure (LBNP or LBPP, respectively) on lung function. Such a maneuver alters thoracic blood volume without the aforementioned changes and does not cause respiratory muscle fatigue or bronchoconstriction, which can be seen with exercise in some individuals, and thus alter spirometric volumes. In addition to the question of the cause of lung volume changes, it is not known whether the changes are constant or related to body size since none of aforementioned investigations studied this (4,5,17,21,23,25,26). Finally, it could be argued that a change in pulmonary blood volume alters pulmonary function not just by shifting blood volume, but by engorging pulmonary vessels and causing a stiffening of the pulmonary parenchyma. Therefore, pulmonary compliance was also measured to help assess whether the changes in pulmonary function caused by lower body pressure changes were strictly a result of a redistribution of blood to the thorax or could be caused by a change in compliance of the lungs.
The experiments in this study were thus designed to test three hypotheses. First, LBPP would lead to a decrease in lung volumes, while LBNP would have the opposite effect. The explanation for this hypothesis is that LBNP would be expected to decrease thoracic blood volume, with LBPP increasing it. Second, the effects of lower body pressure changes on FVC and forced expiratory volume in 1 s (FEV1.0) would be larger in subjects with larger lung volumes. This is because the larger blood volumes in bigger subjects (who would also have larger lung volumes) would be expected to allow a greater absolute shift in blood to or from the thorax. Finally, the effects seen would be a result of changes in thoracic blood volume and not effects on the mechanical properties of the lungs themselves.
A total of 28 healthy subjects were recruited for the three parts of this study (16 males, 12 females, ages 19-41 yr). All were screened for possible respiratory disease via standard spirometry and health history as recommended by the American Thoracic Society (ATS) (1). Criteria for exclusion from the study included a history of cardiovascular or pulmonary disease, resting hypertension (>130/90), or preliminary spirometric evaluations that did not meet the standards associated with healthy pulmonary function (FVC or FEV1.0 <80% predicted or FVC/FEV1.0 ratio <80%). No subjects were excluded on the basis of these guidelines. All subjects were familiar with the testing procedures and signed informed consent forms before any testing, which were approved by the Universities' Institutional Review Boards.
Study 1: Effect of lower body pressure changes on spirometric volumes. The purpose of the first study was simply to determine whether changing thoracic blood volume had an effect on spirometric volumes independent of postural alterations. Seven subjects (four male, three female, ages 22-38 yr) recruited from among laboratory personnel were used for this study. Each subject underwent two trials. In one trial the subjects were fitted into an airtight box in the supine position and sealed at the level of the greater trochanter with a neoprene gasket. Their feet were elevated 1.5 inches on boards to keep the subjects from bending their knees and resisting the blood volume shifts through muscle contraction, while boards were placed between the bottoms of the feet and the end of the box to prevent subject movement. In the other trial, the subjects were fitted into the box in the seated position and sealed at the same level, and the back was supported at a comfortable angle (75°). The back support prevented the subjects from being pushed out of the box with positive pressure application as well as aiding in subject comfort. Positions were chosen as described so that the effect of pressure alterations could be assessed where they were likely to have the most effect. That is, in the supine position there is a larger amount of blood in the thorax than in the upright position, so LBNP draws blood to the lower extremities. While in the seated position, thoracic blood volume is lower, so LBPP forces leg blood into the upper body. In this way, the effect of lower body pressure changes were investigated in either posture. The trials were presented to the subjects in random order.
Upon getting positioned in the box, the subjects were allowed approximately 5 min of rest, after which they performed at least three forced exhalations on a Collins (Braintree, MA) 13.5 water-filled spirometer. Subjects were instructed to keep their heads and shoulders in contact with the table in the supine position and their shoulders on the seat back while in the seated position during all spirometry measurements. While tidal breathing on the spirometer, subjects were instructed to inhale as fully as possible and exhale as hard as possible to residual volume. Measurements were considered valid when they met ATS guidelines for spirometry, i.e., < 200 mL difference between tests, with plateaus at the beginning and end of each spirogram (1). In practice, the differences between spirograms in each trial at rest averaged approximately 50 mL.
After initial spirometry measurements were made, LBPP of 30 mm Hg was applied during the seated test or LBNP of −30 mm Hg was applied during the supine test and subjects rested for 5 min, after which time they began performing spirometry measurements again. As before, at least three spirograms were made. All trials during the periods of altered lower body pressure were completed by the 12th minute of pressure application, after which box pressure was returned to ambient conditions. Five minutes was selected as the waiting period for spirometry measurements to commence during the pressure administration and afterward because preliminary testing showed that FVC changed dramatically in the first minute of pressurization or depressurization, changed less during minutes 2-4, then ceased changing. The pressures applied (± 30 mm Hg) were chosen based on preliminary work in the laboratory in which 20 mm Hg pressures yielded varying results, and 50 mm Hg was not comfortable for some subjects.
After pressure was returned to ambient level, subjects remained in the same position for another 5 min, at which time spirometry measurements were again made.
As a check to determine whether the change in box pressure altered the position of the abdominal contents and thus respiratory muscles, the influence of pressurizing the box on the thoracic and abdominal cavity pressures (esophageal and gastric pressures, respectively) were recorded on two subjects while fitted in the box with no pressure and ± 30 mm Hg of pressure applied. Transdiaphramatic pressure, the difference between esophageal and gastric pressures, was not changed with the box pressures used in this study, implying that abdominal contents did not move with application of box pressure. Additionally, the box was sealed at the greater trochanter, as mentioned above, meaning that the opening was away from the abdomen, so the gasket did not touch the trunk of the subjects.
From each spirogram, FVC and FEV1.0 were determined. These values were subjected to a one-way ANOVA with repeated measures across time (rest, pressure, recovery). P values of less than 0.05 were considered significant.
Study 2: Relation of lung volume change to initial lung volume. The purpose of this part of the study was two-fold. First, we wanted to replicate Study 1 with a group of subjects not used to making pulmonary function measurements. Such a test should give an indication of the robustness of the effect of thoracic blood volume change on pulmonary function. Second, we wanted to determine whether the responses were similar among a wide variety of sizes of subjects. Since both blood and lung volumes vary with height, we would expect the thoracic blood volume shifts to vary with height or initial lung volume as well. Sixteen subjects (nine female, seven male, age 19-31 yr) were recruited from graduate and undergraduate classes. None of the subjects had been trained in respiratory maneuvers before the testing. Five of the subjects repeated the previous study as outlined above. The other 11 subjects performed only the supine test with LBNP added. All procedures and time frames were as described in Study 1. After compilation of data, a one-way repeated measures ANOVA was performed as above. Regression analysis compared the change in FVC or FEV1.0 to the initial spirometric measure for the subject, with Pearson's R used to determine significant correlations.
Study 3: Effect of thoracic blood volume changes on pulmonary compliance. A change in thoracic blood volume might be expected to do more than displace air space; it could engorge vessels and change compliance, thus altering lung volumes and flow rates. Therefore, the purpose of the third part of the study was to measure pulmonary compliance during changes in lower body pressure to help determine which mechanism was responsible for the changes in spirometric parameters seen with altered thoracic blood volume. Five men (age 21-41 yr) were used as subjects for this study. All had participated in one of the first two studies.
Subjects came to the laboratory twice for this study. In the first session, they practiced the breathing maneuvers necessary to make the measurements. Since all had participated in one of the previous studies, preliminary spirometry measurements or practice to show how the LBPP felt were not performed at this time. On the second visit, all measurements were made. Subjects had esophageal balloons inserted into the lower one-third of the esophagus as determined by pressure measurements. They were then placed in the pressure box in the seated position and sealed as before. Only the seated position was used in this study because work by other authors has shown that esophageal pressures measured in the supine position do not reflect intrapleural pressures as accurately as do those in the seated or upright position (19).
After approximately 5 min of rest, the compliance measurements were made. Pressures and volumes were measured simultaneously on separate breaths in which the subject had started at functional residual capacity (FRC) and inhaled maximally, then exhaled to the volume required (range FRC to 2.0 L above FRC) for that breath while the glottis was kept open. In this manner, 4-6 pressure-volume measurements were made on the descending limb of the pressure-volume curve. After approximately 5 min of rest, the measurement was repeated. Following the two measurements under normal conditions, LBPP of 30 mm Hg was applied and two measurements were made under this condition.
The compliance was computed as the slope of the pressure-volume curve, or change in lung volume (above FRC) divided by change in esophageal-minus-airway pressure. All pressure-volume points were combined for each subject under each condition, and one curve was computed for each subject under normal conditions and one under LBPP conditions. The slopes of these curves (i.e., the compliance) were compared by paired t-tests.
Effect of LBNP and LBPP on spirometric volumes. In the supine position, FVC was significantly increased by 0.21 L during LBNP in Study 1 and by 0.13 L in Study 2 (both P < 0.001), while FEV1.0 also increased during LBNP (P < 0.05). When the subjects were seated, LBPP elicited a reduction of 0.17 L in FVC in Study 1 and 0.20 L in Study 2 (P < 0.05 and P < 0.005, respectively). The change in FEV1.0 was not significant in Study 1, but did reach significance in Study 2 (0.2 L reduced, P < 0.005). Both FVC and FEV1.0 returned to resting levels within 5 min of return to atmospheric pressure. These results are shown in Figures 1 and 2.
Effect of size on the change in spirometric volumes. Subjects with the largest FVC values also had, generally, the largest increase in FVC in response to the application of LBNP in the supine position. The correlation between the two variables was significant (r = 0.66, P < 0.01). There was not a significant correlation between the initial FEV1.0 and the change in FEV1.0 in response to LBNP (r = 0.48, P > 0.05). These relationships are graphed in Figure 3.
Effect of thoracic blood volume shifts on pulmonary compliance. The slopes of the pressure-volume relationships were used to calculate compliance. These slopes averaged 0.195 ± 0.030 L(BTPS)/cmH2O (mean ± SEM) under the normal condition and 0.216 ± 0.050 L(BTPS)/cmH2O when the subjects were seated with LBPP applied. These values are similar to those described as "normal" (27) and are not significantly different from each other (t = 0.87, P > 0.1). The individual and group results are shown in Figure 4.
From the results of this study, it is evident that the application of positive or negative pressure to the lower body causes alterations in the FVC and the FEV1.0 consistent with those hypothesized. That is, the application of LBPP decreases vital capacity, while LBNP leads to an increase in FVC. The direction of these changes, along with the absence of changes in transdiaphragmatic pressures from the normal also indicates that the pulmonary effects seen were not caused by the displacement of the viscera with pressure application. Additionally the change in FVC was related to the initial lung volume. This was expected because with increased body size there is an increase in both lung and blood volumes. This would be expected to allow a greater shift of blood with the same pressure application and thus a greater change in lung volume in larger subjects. Finally, the lack of change in pulmonary compliance argues that the effect of LBPP on pulmonary function is to displace blood volume from the lower body to the thorax and not to engorge pulmonary capillaries and increase the stiffness of the lung, which might also decrease the spirometric variables.
Decreases in FVC following exercise of varying intensities and durations have ranged from approximately 100 to 500 mL (4,12,23). This compares favorably with the 170 mL and 200 mL decreases seen in FVC with the application of LBPP in parts 1 and 2 of this study. While the similarities in the change in lung volume between exercise and LBPP may be coincident, they give an indication of the changes likely to take place under either exercise or with elevated thoracic blood volume.
Other investigators have studied the shifts in blood volume with exercise or lower body pressure changes (11,12,15,25). Flamm et al. (13) showed that thoracic blood volume increased by as much as 38% during heavy exercise. This increase was still evident 5 min post exercise, but was returned to normal at 15 min post exercise. They used gamma camera images to estimate changes in the blood pools; thus they did not measure absolute volume changes. However, the time course of the return of thoracic blood volume to normal is comparable with that previously shown in our laboratory (23) for the changes in FVC, which returned to normal within 10-30 min after heavy exercise. Payen et al. (24) showed that under normal breathing conditions the application of 25-40 mm Hg of LBPP increased cardiopulmonary blood volume by about 120 mL. Changes of this magnitude are consistent with both the changes seen in FVC following exercise (4,12) and in the present study during LBPP in parts one and two.
Several studies have shown that vital capacity decreases when a subject shifts from an upright to horizontal position (8,20), is immersed to the chest or neck in water (3,5,25), or breaths against positive or negative pressure (20). One explanation for such changes is an increased thoracic blood volume, as is seen with LBPP. However, shifting from the upright to supine position also results in an upward displacement of the viscera which would decrease FVC. Immersion or resisted breathing may have similar effects on the viscera, but it also places a load on the chest and abdomen, which would also be likely to decrease FVC. Thus, it is difficult to separate the thoracic blood volume effects from other perturbations that might alter FVC using such techniques. Additionally, periodic exposure to microgravity through parabolic flights, which certainly change blood volume distribution, also results in visceral displacement (10).
The use of LBPP or LBNP results in predictable changes in central venous pressure, as shown by previous investigators (6,9), which correlate with changes in central and thoracic blood volumes. It also results in consistent changes in FVC that are most likely related to changes in thoracic blood volume. These results alone would lead us to suspect that exercise-induced increases in thoracic blood volume are a cause of the decreased FVC reported following heavy exercise. The lack of change we saw in pulmonary compliance is similar to those findings of Granath et al. (14), who showed that there was a slight, but insignificant, decrease in compliance in the supine position compared with upright, and no change with exercise. These findings argue that the importance of thoracic blood volume shifts during exercise may be simply to displace air rather than altering the mechanical properties of the lung itself.
However, according to the results of Flamm et al. (13), cycling with only light or moderate loads also leads to increases in thoracic blood volume. They showed that although cycling at a load equivalent to 100% V˙O2max increased thoracic blood volume by 38% whereas loads of 50 and 75% V˙O2max increased thoracic blood volume by 20 and 28%, respectively. Exercise at these intensities does not typically result in altered pulmonary function unless carried out for a prolonged period of time (>2 h) (12). Therefore, the change in thoracic blood volume seen during exercise probably does not account for the full magnitude of the changes seen in lung volumes following heavy exercise. Further studies investigating the impact of other mechanisms, including exercise-induced bronchoconstriction, pulmonary edema, small airways closure, or respiratory muscle fatigue, seem warranted.
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Key Words: LUNG FUNCTION; EXERCISE; THORACIC BLOOD VOLUME; COMPLIANCE
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