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1 Departments of
Anesthesiology, Halliwill, John R., Lori A. Lawler, Tamara J. Eickhoff,
Michael J. Joyner, and Sharon L. Mulvagh. Reflex responses to
regional venous pooling during lower body negative pressure in humans.
J. Appl. Physiol. 84(2): 454-458, 1998.
blood pooling; orthostasis; cardiopulmonary reflex; arterial
baroreflex
LOWER BODY NEGATIVE PRESSURE has been used extensively
to study reflex responses to venous pooling and to test orthostatic tolerance in humans (4, 12). The observation that heart rate responses
to lower body negative pressure are greater than heart rate responses
for negative pressure applied only to the legs (10) suggests that
venous pooling in abdominal or pelvic regions induced by lower body
negative pressure may have major hemodynamic consequences. The
distribution of blood pooling within the lower body during negative
pressure has been studied by measurement of plasma bound
I131 activity and impedence
plethysmography, but results have been mixed. Pooling in the pelvis but
not in the abdomen was seen by Wolthuis et al. (11), whereas pooling in
the pelvis in women and not in men was seen by White and Montgomery
(8). It should be noted, however, that these studies have not addressed
the hemodynamic consequences of venous pooling in the various regions.
Although many areas may pool blood during lower body negative pressure, it is unclear which regions contribute importantly to the overall response. A more thorough understanding of differences in regional contributions to pooling may be relevant to understanding orthostatic intolerance in the general population and in subjects after
interventions such as bed rest or spaceflight.
Therefore, we developed a simple paradigm for assessing the hemodynamic
consequences of regional venous pooling during lower body negative
pressure on the basis of measurements of reflex responses to blood
pooling. We found that hemodynamic responses to lower body negative
pressure when pooling is prevented in the legs (but permitted in the
abdominal and pelvic regions) were nearly equal to responses to
negative pressure when pooling is prevented in all regions. Thus the
hemodynamic consequences of pooling in the abdominal and pelvic regions
during lower body negative pressure appear to be negligible in healthy
individuals.
Sixteen healthy, normotensive, nonsmoking subjects (8 women and 8 men)
between the ages of 18 and 48 yr volunteered for the present study. The
study was approved by the Institutional Review Board, and each subject
gave written informed consent before participating. On a preliminary
visit, subjects were familiarized with the procedures used in the study
and underwent a graded maximal treadmill test to determine maximum
aerobic power (maximal O2 uptake).
The test comprised 2-min workload increments sufficient to achieve
exhaustion within 8-12 min; maximal
O2 uptake values and subject
characteristics appear in Table 1. Subjects
subsequently underwent studies on 3 separate days, separated by at
least 1 wk.
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
Lower body negative pressure is frequently used to simulate
orthostasis. Prior data suggest that venous pooling in abdominal or
pelvic regions may have major hemodynamic consequences. Therefore, we developed a simple paradigm for assessing regional contributions to
venous pooling during lower body negative pressure. Sixteen healthy men
and women underwent graded lower body negative pressure protocols to 60 mmHg while wearing medical antishock trousers to prevent venous pooling
under three randomized conditions:
1) no trouser inflation (control),
2) only the trouser legs inflated, and 3) the trouser legs and
abdominopelvic region inflated. Without trouser inflation, heart rate
increased 28 ± 4 beats/min, mean arterial pressure fell 
3 ± 2 mmHg, and forearm vascular resistance increased 51 ± 9 units at 60 mmHg lower body negative pressure. With inflation of either
the trouser legs or the trouser legs and abdominopelvic region, heart
rate and mean arterial pressure did not change during lower body
negative pressure. By contrast, although the forearm vasoconstrictor
response to lower body negative pressure was attenuated by inflation of
the trouser legs (
forearm vascular resistance 33 ± 10 units,
P < 0.05 vs. control), attenuation was greater with the inflation of the trouser legs and abdominopelvic region (forearm vascular resistance 16 ± 5 units,
P < 0.05 vs. control and trouser
legs-only inflation). Thus the hemodynamic consequences of pooling in
the abdominal and pelvic regions during lower body negative pressure
appear to be less than in the legs in healthy individuals.
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
Table 1.
Subject characteristics and hemodynamic variables
General Procedures
During studies, heart rate was monitored by using a 5-lead electrocardiogram. Arterial pressure was monitored noninvasively on a beat-to-beat basis by using a Finapres blood pressure monitor (model 2300, Ohmeda, Englewood, CO) adjusted to heart level. Breathing was monitored by using a bellows placed around the subject's abdomen.Venous occlusion plethysmography. Forearm blood flow was estimated by venous occlusion plethysmography with a mercury-in-Silastic strain gauge (3). An arterial occlusion cuff around the wrist was continuously inflated to suprasystolic pressures (250 mmHg) during measurements, while a venous occlusion cuff around the upper arm was inflated to 40 mmHg for 7.5 s out of every 15 s, providing one blood flow measurement every 15 s. Forearm blood flow was expressed as milliliters per deciliter of tissue per minute.
Lower body negative pressure. The lower body of the subject was sealed in an airtight box above the level of the iliac crests. The box was attached to a rheostat-controlled commercial vacuum so that graded negative pressures up to 60 mmHg could be rapidly produced. The subject was supported by a bicycle seat mounted within the box.
Medical antishock trousers. Subjects wore segmented medical antishock trousers (Gladiator 3-section antishock pants, Jobst, Toledo, OH), which were configured so that the trouser leg and abdominopelvic regions could be inflated independently. The leg region reached from the malleolus to the base of the pelvis, and the abdominopelvic region reached from the base of the pelvis to above the iliac crests, where the seal for the lower body negative pressure box was located. When in use, the trousers were inflated to 5 mmHg (relative to outside the negative pressure box), which negated superimposed lower body negative pressure. This is not the same way the trousers would work against orthostasis or the way they would be used to treat severe (traumatic) hypovolemia. A low pressure was chosen to avoid activating the reflex observed by Williamson and colleagues (9) and to avoid potential fluid shifts out of the lower body (2).
Experimental Design
Each of the 3 study days was preceded by an overnight stay in the General Clinical Research Center (GCRC), where subjects received a standardized evening meal. After 2400, subjects fasted and received overnight intravenous fluid hydration (saline, 125 ml/h for 8 h) to ensure both adequate and comparable hydration during all studies. Each subject was then studied in the morning at a consistent time (beginning at either 8 or 10 AM). All subjects were advised to refrain from alcohol and exercise in the 12 h before GCRC admission. For the study, subjects donned medical antishock trousers and were instrumented while in the supine position within the lower body negative pressure box. Subjects then underwent a ramped, graded lower body negative pressure protocol while heart rate, arterial pressure, forearm blood flow, and respiration were monitored. During the lower body negative pressure protocol, the medical antishock trousers were used to negate the effect of lower body negative pressure on either 1) the legs only or 2) the legs and abdominopelvic region. These two conditions and a control condition (no trouser inflation) were randomized across the 3 study days.Lower body negative pressure protocol. After instrumentation, the subject rested for 10 min. Figure 1 shows the time line for the following protocol. After a 5-min baseline period, the medical antishock trousers were inflated in a random manner (i.e., no inflation, trouser legs only, or trouser legs and abdominopelvic region) and a second 5-min baseline period was observed. Then, lower body negative pressure was applied continuously and sequentially at levels of 10, 20, 30, 40, 50, and 60 mmHg for 5 min at each level, whereas the trouser condition remained constant throughout the ramp. After the last period of negative pressure, two 5-min recovery periods were observed. Measurements were made during the last 2 min of each period. The negative pressure protocol was terminated if the subject exhibited presyncopal signs or symptoms (e.g., lightheadedness, nausea, hypotension, bradycardia, or loss of consciousness).
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Data Analysis
Data were digitized and stored on a computer at 1,000 Hz and were analyzed off-line with signal-processing software (WinDaq, Dataq Instruments, Akron, OH). After the R-R intervals were determined from the electrocardiogram, the data were decimated to 100 Hz for derivation of arterial pressure and blood flow. Mean arterial pressure was derived from the arterial pressure waveform. Forearm blood flow was determined from the derivative of the forearm plethysmogram. Forearm vascular resistance was calculated as (mean arterial pressure)/(forearm blood flow) and was expressed as units.Statistics. Because the data fit a normal distribution (Wilk-Shapiro test), parametric analysis was used. Unpaired t-tests were used to compare the subject characteristics across gender. Repeated-measures analysis of variance was used to compare baseline responses to trouser inflation across all three conditions and to compare responses to the lower body negative pressure protocol across all three conditions. Significant (P < 0.05) effects and interactions were further analyzed by using Fisher's least significant difference test. All values are reported as means ± SE.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Baseline Values
Table 1 shows the subject characteristics by gender. Because the baseline hemodynamic values recorded on the three visits did not differ, the mean of the three baselines is presented. Baseline hemodynamic values did not differ between men and women, although forearm blood flow tended to be higher and forearm vascular resistance tended to be lower in men than in women. Because there were no differences between men and women in the responses to lower body negative pressure across conditions, the data from men and women were combined.Responses to inflation of medical antishock trousers. Inflation of the trousers, completely or partially, did not alter the hemodynamics measured during the second baseline (see Table 2). Therefore, responses were analyzed as changes from the second baseline, which would reflect the consequences of lower body negative pressure alone. A key observation was the lack of forearm vasodilation at baseline when the trousers were inflated, suggesting that trouser inflation did not produce an increase in central blood volume (6, 7).
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Responses to Lower Body Negative Pressure
Reflex responses to venous pooling (all regions).
Figure 2 shows the mean response in all 16 subjects to lower body negative pressure during the control condition,
without trouser inflation (
). During graded lower body negative
pressure, heart rate increased from baseline by the 40-mmHg negative
pressure stage (58 ± 2 vs. 67 ± 2 beats/min,
P < 0.05) and continued to rise (86 ± 5 beats/min at 60 mmHg negative pressure,
P < 0.05). Mean arterial
pressure decreased from baseline by the 20 mmHg stage (85 ± 2 vs.
83 ± 2 mmHg, P < 0.05) and
continued to fall (81 ± 3 mmHg at 60 mmHg negative pressure,
P < 0.05). Forearm vascular
resistance increased from baseline by the 20 mmHg stage (50 ± 6 vs.
71 ± 10 units, P < 0.05) and
continued to rise (101 ± 13 units at 60 mmHg negative pressure,
P < 0.05).
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Reflex responses to venous pooling (legs excluded).
Figure 2 shows the mean response in all 16 subjects to lower body
negative pressure during the legs-only condition, with only the trouser
legs inflated (
). During graded lower body negative pressure, heart
rate and mean arterial pressure did not change compared with baseline
(P > 0.05). Forearm vascular
resistance increased from baseline by the 30 mmHg stage (52 ± 5 vs.
64 ± 7 units, P < 0.05) and
continued to rise (85 ± 12 units at 60 mmHg negative pressure,
P < 0.05).
Reflex responses to venous pooling (legs and abdominopelvic regions
excluded).
Figure 2 shows the mean response in all 16 subjects to lower body
negative pressure during the legs and abdominopelvic region condition
[all regions of the trousers inflated (
)]. During graded lower body negative pressure, heart rate and mean arterial pressure did
not change compared with baseline (P > 0.05). Forearm vascular resistance increased from baseline by the
30 mmHg stage (50 ± 6 vs. 61 ± 8 units,
P < 0.05) and continued to rise (68 ± 12 units at 60 mmHg negative pressure,
P < 0.05).
Differences between conditions. The responses to lower body negative pressure depended on which regions of the trousers were inflated (see Fig. 2). When the trousers were not inflated, changes in mean arterial pressure, heart rate, and forearm vascular resistance were greater (P < 0.05) than those for the two conditions in which the trousers were inflated completely or partially (asterisk in Fig. 2). When the trousers were inflated, changes in forearm vascular resistance were greater when only the trouser legs were inflated compared with when both the trouser legs and abdominopelvic region were inflated, but only at the 60-mmHg lower body negative pressure stage (P < 0.05, Fig. 2B).
Presyncopal episodes.
A total of six subjects (nonfinishers) was unable to complete the lower
body negative pressure protocol during the control condition (no
trouser inflation) due to the development of presyncopal symptoms or
frank syncope. Two men and two women stopped during the 60-mmHg stage,
whereas one woman stopped during the 50-mmHg and one during the 40-mmHg
stage. None of the subjects developed presyncopal symptoms when the
trousers were inflated completely or partially. In general, when the
trousers were inflated the nonfinishers showed the same trends as the
finishers. However, at the 60-mmHg lower body negative pressure stage,
nonfinishers had a higher heart rate when only the trouser legs were
inflated compared with when both the trouser legs and abdominopelvic
region were inflated (heart rate: 4 ± 3 vs. 0 ± 1 beats/min,
trouser legs inflation vs. trouser legs and abdominopelvic inflation, P < 0.05).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The novel finding of this study is that the hemodynamic consequences of venous pooling in the abdominal and pelvic regions during lower body negative pressure appear to be negligible in healthy individuals. We found that, by selectively preventing venous pooling in the legs, the reflex tachycardia and vasoconstriction seen during lower body negative pressure could be greatly attenuated. When we also prevented pooling in the abdominopelvic region, this further attenuated the vasoconstrictor response, but only at high levels of lower body negative pressure. Thus many areas may pool blood during lower body negative pressure, but it appears that the legs contribute most in the overall response to lower body negative pressure.
Previous Studies
Previously, Wolthuis et al. (11) measured changes in the distribution of plasma bound I131 activity during 40 mmHg lower body negative pressure and suggested that significant pooling occurs in the foot, calf, thigh, buttock, and pelvis, but not in the abdomen. In fact, they were able to demonstrate a 20% rise in activity in the pelvis (compared with a 54% rise in the calf and a 0.2% decline in the abdomen). More recently, White and Montgomery (8) measured changes in electrical impedence during acute nonramped 50 mmHg lower body negative pressure and suggested that significant pooling occurs in the pelvis in women but not in men. However, although both studies suggest that venous pooling may occur in the pelvis during moderate to high levels of lower body negative pressure, they do not address the physiological significance of pelvic blood pooling.In support of the significance of abdominopelvic pooling, Wolthuis et al. (10) found heart rate responses to lower body negative pressure (50-60 mmHg) were greater than responses to leg negative pressure alone. In contrast, we only found evidence for physiologically significant blood pooling in the abdominopelvic region during unphysiologically high levels of lower body negative pressure (60 mmHg). These differences may be due to the limited number of subjects (n = 4) studied by Wolthuis et al. or differences in the experimental conditions. Wolthuis et al. relied on separate boxes for producing lower body negative pressure and leg negative pressure; it is unclear whether this could account for the differences between their and our results.
Limitations
Lower body negative pressure has been used extensively to simulate orthostasis and to assess orthostatic tolerance; however, lower body negative pressure is not identical to orthostasis. In true orthostasis, a hydrostatic pressure gradient exists from the level of the heart to the feet, whereas lower body negative pressure exerts a uniform distending pressure on all regions within the chamber. Thus, in our lower body negative pressure protocol, the feet, legs, pelvis, and abdomen are all exposed to a 60-mmHg increase in distending pressure. In true orthostasis, the feet may experience distending pressure increases of ~70 mmHg, but the abdomen and pelvis will experience much less due to their proximity to heart level (probably <10 mmHg, on the basis of femoral venous pressure) (5). Therefore, a limitation of our study is that the distending pressures at which we saw an abdominopelvic contribution to the vasoconstriction (60 mmHg) are not exerted on the abdominopelvic vasculature during true orthostasis. Thus the physiological contribution of this vascular region to orthostatic stress may be even less than our results suggest.Another limitation is that we did not directly measure the effect of venous pooling in the leg region but indirectly assessed it by contrasting the effects of abdominopelvic pooling with combined leg and abdominopelvic pooling. Had the abdominopelvic area been excluded, with the legs exposed to negative pressure, it is possible that the effect would have been similar to the trial with the legs excluded. However, prior observations of reflex reponses to isolated leg negative pressure suggest this is not the case (7).
Perspectives
Differences in regional contributions to blood pooling may be relevant to understanding orthostatic intolerance in the general population and in subjects after bed rest or spaceflight. Our results suggest that orthostatic tolerance in normal individuals is more likely to be affected by changes in venous compliance in the legs than in the abdominopelvic region. Thus attempts at preventing the rise in leg compliance that is associated with bed rest and spaceflight are warranted (1). Furthermore, attempts at reducing leg venous compliance are likely to be efficacious in treating orthostatic intolerance in the general population.It is conceivable, however, that abnormalities in the abdominal or pelvic vasculatures could play a role in the pathophysiology of orthostatic intolerance in some instances. In partial support of this concept, we noticed some differences in the heart rate responses between finishers of our lower body negative pressure protocol and nonfinishers. Along these lines, we speculate that if the abdominopelvic region is more important in orthostatic-intolerant people, then affected individuals would demonstrate a greater susceptibility to lower body negative pressure than to upright tilt, due to the differing pressure distributions of the two testing modalities.
In summary, the legs appear to be the predominant site of venous pooling during lower body negative pressure in normal humans. We found that venous pooling in the abdominopelvic region contributed little to the overall hemodynamic effects of lower body negative pressure in humans. These observations underscore the need to understand the factors that affect compliance of the leg vasculature.
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ACKNOWLEDGEMENTS |
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We thank Darrel L. Loeffler, Robin A. Horn, Stacey A. Vlahakis, and Jolene M. Summer for technical assistance. We especially thank the subjects who volunteered for these studies.
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FOOTNOTES |
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These studies were supported by National Institutes of Health Grants M01-RR-00585, RR-00585-24, NS-32352-01, and HL-46493, the Glen L. and Lyra M. Ebling Cardiology Research Endowment, and the Mayo Foundation.
Address for reprint requests: S. L. Mulvagh, Cardiovascular Div., Mayo Clinic, W-16B, 200 First St. SW, Rochester, MN 55905 (E-mail: mulvagh.sharon{at}mayo.edu).
Received 9 June 1997; accepted in final form 15 September 1997.
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REFERENCES |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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