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Gravitational Research Branch, NASA Ames Research Center, Moffett Field, California 94035-1000
Submitted 25 February 2003 ; accepted in final form 1 February 2004
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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36% of supine baseline levels. Flow increased back toward baseline levels at 80–100 mmHg LBNP yet remained stable during 0.8–1.0 Gz tilt. Centrifugation usually produced less leg vasoconstriction than tilt or LBNP. Surprisingly, SAC and LAC did not differ significantly. Thigh responses were less definitive than leg responses. No gravitational vasoconstriction occurred in the neck. All conditions except SAC increased heart rate, according to our hypothesized order. LBNP may be a more effective and practical means of simulating cardiovascular effects of gravity than centrifugation. gravity; cutaneous circulation; hemodynamics; short- and long-arm centrifuges; microgravity countermeasures; lower body negative pressure
Peripheral vasoconstriction during orthostasis is mediated centrally by adrenergic activation in response to unloading of arterial and cardiopulmonary baroreceptors; the vasoconstriction reduces blood flow in the cutaneous, muscular, splanchnic, and renal circulations (4, 27). In addition to baroreflex control, vasomotor tone is also increased by local mechanisms such as myogenic autoregulation (20) and cutaneous venoarteriolar reflexes (18, 19). These mechanisms increase vascular resistance in response to elevated local arteriolar and venular pressures, respectively (16, 18). Cutaneous vasoconstrictor responses to orthostasis vary along the length of the body: lower extremity sites consistently vasoconstrict during orthostasis, whereas upper body sites do not (2, 4, 14). Therefore, local mechanisms react to the gravitational pressure gradient and complement baroreflexes in mediating the peripheral vascular response to orthostasis (4, 19). We speculate that preservation of these collective responses will facilitate preservation of orthostatic tolerance during spaceflight.
Centrifugation and lower body negative pressure (LBNP) simulate cardiovascular effects of gravity; each have been proposed as countermeasures against cardiovascular deconditioning during long-duration spaceflight (6, 7, 15, 31). Although these artificial measures can elicit systemic cardiovascular reactions qualitatively similar to those of upright posture (14), they generate quantitatively distinct distributions of vascular transmural pressure along the body (Fig. 1) and should, via reflex adjustments and local autoregulation, elicit different magnitudes and distributions of microvascular response. For tilting and centrifugation, local arterial pressure change from Gz stimulation is calculated as pressure (P) at a distance h from the arterial hydrostatic indifference level, applied along the z (head to feet) body axis, according to the following expressions
 | (1) |
 | (2) |
is the density of blood (assumed 1.05 g/cm3), g is the acceleration of gravity, 
is the tilt table angle from horizontal, rh is the radial position of the subject's arterial hydrostatic indifference level from the centrifuge axis, and 
is the centrifuge angular velocity. For LBNP, lower body arterial transmural pressure equals mean arterial pressure plus applied negative pressure (1, 23).
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In the present study, we compared true orthostasis (whole body head-up tilt) and three simulated orthostatic stimuli [supine short-(SAC) and long-radius +Gz centrifugation (LAC), and supine LBNP] in terms of the cutaneous microvascular blood flow responses along the length of the body, as well as heart rate and blood pressure responses. Similarly to other workers (17, 25), we equalized gravitational stress across stimuli at the level of the feet. We hypothesized that the gravitational stimuli elicit local cutaneous and systemic responses in the following order, from lowest to highest response: SAC, LAC, tilt, and LBNP. We based these expectations on the arterial vascular transmural pressure profiles generated by the Gz stimuli, as predicted by Eqs. 1 and 2 and illustrated in Fig. 1.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Regional cutaneous microvascular blood flow was assessed by three laser-Doppler flowmeters (BPM 403A, Vasamedics, St. Paul, MN) that measure microvascular flow in 1 mm3 of tissue in linear but arbitrary units (24). Laser-Doppler probes were attached by two-sided adhesive tape at the lateral neck (midway between angle of mandible and medial clavicle), anterior thigh (midpoint between perineum and superior aspect of patella), and anterior tibial region at the level of maximal calf girth. Instrument averaging time was set to 1 s.
Arterial blood pressure and heart rate were measured continuously by an automatic finger cuff blood pressure monitor (Finapres 2300, Ohmeda, Boulder, CO). An arm sling supported the arm and held the finger in which blood pressure was measured at heart level. Diastolic pressures from the automatic system were verified by arm cuff sphygmomanometry on the contralateral arm.
All instrument outputs were digitized continuously (sampling frequency 2 Hz; 20 Hz for blood pressure) with a portable microcomputer (SupersPort; Zenith, St. Joseph, MI) equipped with data-acquisition hardware (DAS-20; Metrabyte, Taunton, MA) and software (Labtech Notebook; Laboratory Technologies, Wilmington, MA).
On separate days, and in a predetermined counterbalanced random order unique for each, subjects underwent each of the following four experimental treatments (Fig. 1): whole body tilting, LAC, SAC, and LBNP.
Whole body tilting. Subjects were placed on an electric tilt table in the supine position. A restraining strap placed across the upper abdomen secured subjects against the tilt table surface during upright tilt. It applied negligible pressure to the body surface. The tilt table rotated around an axis located 0.5 m behind the thighs of subjects.
LAC (foot radial position: 8.5 m). Subjects were placed supine in the centrifuge cab with the head oriented toward the rotational axis. All subjects' feet were placed at the same distance from the axis, and head radial position depended on subject height. The interior of the centrifuge cab was painted black and sealed completely from external light, protecting subjects from any visual cues of rotation. Dependent on individual heights, subjects were exposed to an 25% Gz gradient defined as
 | (3) |
and 
are centripetal accelerations at the foot and head, respectively, along the length of the body.
SAC (foot radial position 2.4 m). The same configuration as LAC was employed except for foot radial position. Subjects experienced an 75% Gz gradient from foot to head.
LBNP. Subjects were placed supine into a LBNP chamber and sealed with a rubber gasket and waist belt at the superior iliac crest. Blood pressure was measured at the arm at each LBNP level.
The stepwise testing protocol for each treatment is summarized in Table 1. Stepwise levels of each treatment were chosen to produce comparable levels of Gz at the feet. For the purpose of the present study, LBNP at 100 mmHg was considered comparable to upright tilt on Earth in terms of the similarity of foot-level vascular transmural pressures exerted by these two procedures (1, 14). We chose to equalize gravitational stimulation at foot level also because it permits simple standardization across subjects and conditions, and because equalization at a higher anatomic level (e.g., heart or head) would approach or exceed the revolutions per minute capability of our SAC.
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For all treatments, subjects' feet were positioned against a foot-plate. In all cases, baseline and recovery data were recorded for 1 min before and 5 min after each procedure, respectively. Each stimulus level was maintained for 30 s; transitions between stimulus levels were 10 s in duration. Subjects were instructed to remain relaxed and quiet throughout all studies, and they were monitored for any signs of presyncope during all tests. For familiarization, on a day before data collection, all subjects underwent each protocol with only medical monitoring instrumentation. Time of day of testing was controlled within 1 h for each subject.
Room temperature was maintained at 23 ± 0.5°C. Subjects wore a T-shirt, shorts, and socks. Air flow over subjects' skin was controlled, in that no air conditioning or heating drafts were allowed, and the LBNP chamber and centrifuge cabs were well sealed to minimize air movement in those enclosures.
Flowmeter readings achieved stable levels within 10 s after each transition; flowmeter outputs, heart rate, and blood pressure were averaged over the last 10 s of each 30-s stimulus interval. Two-factor repeated-measures ANOVA was used to determine effects of Gz stimulus and stimulus level for each skin blood flow measurement site and for heart rate and blood pressure. Least significant difference post hoc tests were used to determine differences between flow responses and baseline control. Paired t-tests of percent changes from baseline were used for post hoc assessment of Gz stimulus differences at specific Gz levels. Because of the large number of post hoc tests, we employed a probability level of 0.01 to reduce chances of falsely rejecting the null hypothesis. In all other statistical tests, a probability level of 0.05 was considered significant. For presentation, flowmeter signals for each subject were normalized to the mean level present at initial supine baseline and shown as percentages of that baseline. Means and standard errors are shown for each dependent variable. StatView software (version 5.0 for Windows; Cary, NC) performed statistical tests.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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In general, for real and artificial gravitational stimuli, application of increasing Gz levels progressively reduced cutaneous microvascular blood flow in the lower extremity. However, neck skin blood flow exhibited no response to Gz stimulation, regardless of the source of stimulation (P > 0.9; Fig. 2).
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All four stimuli significantly decreased thigh cutaneous blood flow, but differences appeared in the Gz levels of the various stimuli that produced decreases and between the degree of reduction elicited by the stimuli at given Gz levels (Fig. 3). All levels of tilt and LBNP (0.2–1.0 Gz, 20–100 mmHg LBNP) significantly reduced thigh skin blood flow (P < 0.006), but LAC reduced blood flow only at levels >0.2 Gz (P < 0.002), and SAC only at level 0.6 Gz or greater (P < 0.01). Thigh skin blood flow decreased more during LBNP at 0.2–0.4 Gz than during all other stimuli during Gz onset (P < 0.002), and LBNP remained different than both forms of centrifugation, but not tilt, at 0.6–0.8 Gz (P < 0.001). Thigh skin blood flow during tilt was less than during SAC at 0.4–0.8 Gz and less than during LAC at 0.6 Gz (P < 0.001). At 1.0 Gz, only tilt and SAC differed significantly in terms of thigh skin blood flow (P = 0.003). Thereafter (0.8 down to 0.2 Gz), thigh skin blood flow during tilt and LBNP remained less than that during SAC (P < 0.01). LAC closely approximated tilt from 1.0 to 0.2 Gz and did not differ significantly from any other condition in this range. All differences disappeared on return to 0 Gz.
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Leg skin blood flow differed more clearly between conditions than did thigh skin blood flow. Tilt, SAC, and LBNP all significantly reduced leg skin blood flow at all ascending and descending Gz levels (P < 0.005; Fig. 4). Surprisingly, significant effects of LAC appeared only from 0.6 Gz (ascending) through 0.2 Gz (descending) (P < 0.007). Tilt and LBNP produced similar leg skin blood flow responses except at 1.0 Gz, at which flow during LBNP increased back toward baseline, and thus tended to differ from tilt responses (P = 0.041). At 1.0 Gz, LBNP, LAC, and SAC responses were similar. At 0.4–0.6 Gz (ascending and descending), tilt and LBNP reduced skin blood flow more than both forms of centrifugation (P < 0.009), and a similar trend appeared at other Gz levels. Surprisingly, SAC tended to decrease leg skin blood flow more than LAC at 0.4 Gz (P < 0.04), and this trend remained consistent across Gz levels except at the final 0.2 Gz exposure. As at the thigh, no differences from baseline or between conditions persisted after return to 0 Gz.
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LBNP resulted in the greatest heart rate response, followed by tilt and LAC (Fig. 5). Heart rate increased significantly for LBNP at 0.4 Gz, tilt at 0.6 Gz, and LAC at 0.8 Gz (P < 0.01). No heart rate response appeared during SAC. During baseline conditions before LBNP, heart rate tended to exceed that seen before other conditions (P < 0.033). Heart rate during LBNP significantly exceeded that during all other conditions at all Gz levels (P < 0.002) except 0.2 descending. Heart rate during tilt significantly exceeded that during LAC at 0.8–1.0 Gz (P < 0.001); heart rates during tilt and LAC exceeded those during SAC at 0.6 and greater Gz ascending, and 0.8 Gz descending (P < 0.004). Tilt significantly increased mean arterial pressure at 1.0 Gz (P < 0.005), but no other experimental condition changed arterial pressure (Fig. 6). Arterial pressure during tilt significantly exceeded that in other conditions at 0.6 and greater Gz (P < 0.01). No other differences in arterial pressure appeared between conditions.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Lower extremity cutaneous vasoconstriction with gravitational stimulation. All gravitational stimuli elicited lower extremity vasoconstriction, and the relative vasoconstriction between stimuli followed our expectations to some extent. For example, the onset of thigh vasoconstriction matched the above hypothesis. However, vasoconstriction during LAC never exceeded that during SAC at given Gz levels and in fact tended to be less than during SAC at the leg. We expected lower extremity vasoconstriction during LAC to exceed that during SAC primarily because of the higher calculated lower extremity arterial pressures during LAC (Fig. 1). These higher local vascular pressures should have activated local venoarteriolar and myogenic reflexes more during LAC than SAC. LAC should also have unloaded central and arterial baroreceptors, and therefore activated baroreflexes, more than SAC, although this is more speculative. The trend for leg vasoconstriction to be less during LAC than SAC is surprising and interesting, but we offer no speculation for it.
Tilt and LBNP generated more similar responses at the leg than at the thigh. This may be because LBNP more closely approximates local vascular pressures produced by tilt at the leg than at the thigh, at least with Gz equalized at the level of the feet (Fig. 1). Similar local vascular pressures at the leg should have similarly activated local venoarteriolar and myogenic reflexes. At the thigh, LBNP transvascular pressures theoretically exceed those during tilt at the same foot-level Gz (Fig. 1), which should lead to greater local reflexive vasoconstriction during LBNP, as we saw during Gz onset. In the present experimental conditions, an asymptotic "floor" of cutaneous vasoconstriction occurred at 30% of supine resting blood flow for both thigh and leg.
At 100 mmHg LBNP (simulated 1.0 Gz), skin blood flow increased back toward baseline levels at both lower extremity sites. This microvascular flow increase could represent enhanced capillary recruitment due to mechanical microvascular distension from negative tissue pressures. In the lower body microcirculation, an important qualitative distinction exists between the acceleration stresses and LBNP. During upright posture, and presumably centrifugation, hydrostatic pressure elevation in lower body capillary networks equals only 75% of that seen in the arteries and veins, due to increased arterial resistance (22). In contrast, the stress of LBNP is transmitted equally to all segments of the enclosed circulation, including the microvasculature (1). This recruitment effect appears to have offset partially the flow-reducing effect of upstream vasoconstriction. Furthermore, enhanced capillary recruitment increases surface area for capillary filtration and therefore facilitates extravascular fluid accumulation in the lower body during LBNP (1).
Lack of response to Gz stimuli at the neck. The lack of vasoconstrictor response in the neck with orthostatic stimulation agrees with our previous findings (4). Jepsen and Gaehtgens (19) and the present results demonstrate a stronger orthostatic vasoconstriction response in the lower vs. upper body. Moreover, both studies imply that central and local regulatory mechanisms interact to mediate local blood flow changes in response to gravitational stimulation. Gravitational pooling is largely a lower body problem: less need exists for vasoconstrictive mechanisms to prevent pooling in the upper body. In fact, any such upper body vasoconstriction could be counter-productive to maintenance of blood flow there during gravitational stress, owing to reduced local perfusion pressure (Fig. 1).
Some studies suggest a predilection for the neck cutaneous microcirculation to vasodilate relative to other skin regions. Topical benzoic acid increased neck skin blood flow more than at the face or forearm (28). During total immersion in cool (25°C) water, heat loss from the neck exceeded that from other sites (30), suggesting less thermoregulatory vasoconstriction at the neck than at other areas.
Heart rate responses to Gz stimuli. Gz stimulation increased heart rate according to our hypothesized pattern: SAC, LAC, tilt, and LBNP (from lowest to highest response). Stimulus-induced unloading of arterial and low-pressure baroreceptors (11, 12) and baroreflex interactions (10, 13) probably increased heart rate according to the hypothesized order. However, we report no data directly assessing differential effects of the various Gz stimuli on baroreceptor unloading, venous volume redistribution, or baroreflex interactions, so we draw no firm conclusions concerning these factors.
We are unsure why heart rate before LBNP exceeded heart rate before other experimental conditions. LBNP was the only experimental condition in which the lower body was enclosed in a chamber, and it was the only condition during which the medical monitor was at the subjects' side during testing. We do not believe this 7–8 beat/min baseline heart rate disparity importantly affected subsequent responses or the overall integrity of these data for testing our hypotheses.
The complete lack of heart rate response to SAC surprised us. An explanation may lie in how centrifugation affects blood pressure at the baroreceptors. In contrast to upright posture (tilt), centrifugation applies a nonuniform acceleration along the length of the body. This gradient creates quantitative differences in the distribution of blood pressures (Fig. 1) and consequently the cardiovascular response. Carotid baroreflex stimulation during Gz acceleration involves a reduction in pressure at the carotid sinus relative to the heart. In upright posture on Earth, the gradient of arterial gravitational pressure along the length of the body is constant. In contrast, pressure exerted by centripetal Gz acceleration increases from head to foot (Fig. 1). Because the arterial baroreceptor system is located near the top of the hydrostatic column, this region experiences a smaller pressure change during centrifugation compared with whole body tilting when gravitational and centripetal accelerations are equalized at foot level, as in our study.
This implies that a centrifuge, especially one of short radius, may be disadvantageous for baroreflex stimulation, a concept supported by the lack of observed changes in heart rate during SAC. Theoretically, for a 180-cm-tall person, it would be necessary to rotate a 2.4-m-radius centrifuge (our SAC) to 2.5 Gz at the feet (30 rpm) to achieve a similar hydrostatic reduction in neck (carotid sinus) blood pressure as upright standing posture. In a 1.8-m-radius centrifuge (head at rotational axis, 100% Gz gradient), the required foot-level acceleration increases to 5 Gz (50 rpm). These high accelerations generate theoretical gravitational pressures in excess of 300 mmHg at foot level. This may cause sufficient venous pooling in the legs to reduce systemic arterial pressure by means of reduced cardiac filling pressures, which would indirectly stimulate arterial baroreflexes.
Previous investigations demonstrate that 50 mmHg LBNP produces similar central circulatory conditions to upright standing (e.g., Ref. 35). This holds true in the present results if we interpolate our data between 40 and 60 mmHg LBNP for heart rate and thigh and leg blood flow and then compare to those data at 1.0 Gz tilt. LBNP of 50 mmHg approximates arterial transmural pressure at the upper thigh of an upright adult (Fig. 1). Our results support the traditional contention that 50 mmHg LBNP simulates cardiovascular conditions and responses of upright standing, at least for heart rate and peripheral cutaneous microvascular responses.
Why did arterial pressure increase only during tilt? Heart-level arterial blood pressure increased during tilt but not during any of the other Gz stimuli. This may have been due to some visual or vestibular stimulation unique to tilt. Of the four stimuli, head-up tilt is the only one in which subjects visually perceived movement. Upright tilt also imposes vestibular Gz stimulation with minimal Gx and angular accelerations. Substantial literature demonstrates vestibular system effects on cardiovascular control (3, 21, 26, 34). Such effects may be relatively variable and transient in humans during tilt (32). Nevertheless, upright posture (tilt) may activate vestibular or visual-motor blood pressure control mechanisms that are not activated during supine applications of simulated gravity.
As discussed above for the baroreceptors, the vestibular system is located near the top of the body and therefore experiences a smaller Gz acceleration change during centrifugation (particularly SAC) compared with whole body tilting. For example, a 180-cm-tall supine subject undergoing our LAC at 1 Gz at foot level experiences 0.77 Gz at the level of the otolith organs. During SAC at 1 foot-level Gz, this subject's otolith organs experience only 0.28 Gz. Centrifugation in microgravity would produce similar results. Supine LBNP and LBNP in microgravity at rest produce no otolith Gz stimulation. Also, centrifugation elicits Coriolis forces, whereas upright posture and LBNP do not.
Such differences may well influence blood pressure regulation and may therefore contribute to the different cardiovascular responses seen with tilt, LAC, SAC, and LBNP. Subtle differences in vestibular stimulation affect cardiovascular responses to orthostatic stress (9, 21, 34). For example, Cheung and colleagues (9) demonstrated that blood pressure decreased less when head-down to head-up tilt occurred around the pitch axis than around the roll axis. Vestibular contributions to blood pressure control become important when considering counter-measures for orthostatic intolerance after spaceflight, because evidence exists that vestibular factors may contribute to this intolerance (33).
Limitations. We placed the laser-Doppler flow probes according to the landmarks described in METHODS, but it is unlikely they were placed at exactly the same location for the various conditions on different days. This variability in placement may change absolute levels of flow. However, our laboratory's previous experience with laser-Doppler flowmetry (2, 4, 29) and pilot studies for the present work support day-to-day consistency in relative responses to Gz stimulation with replacement of probes. As discussed above, some differences existed between experimental conditions besides just the source of Gz stimulation (e.g., close-by medical monitor presence only for LBNP, perception of movement only during tilt). We are confident that such factors did not importantly affect the present findings, but they remain potential sources of variability.
Changes in skin temperature influence cutaneous blood flow (8). We did not measure skin temperature. However, we equalized air temperature and subject clothing across conditions, and we controlled air flow by minimizing drafts in all conditions. We believe these precautions minimized opportunity for skin temperature to affect our results, but because we did not measure skin temperature or local air flow, we cannot fully rule out that temperature-related vasoconstriction some-how contributed to the responses we measured.
Although the acceleration exerted by an Earth-bound centrifuge is purely centripetal, and therefore aligned along the z body axis of a supine human, the total acceleration experienced by the subject is the vector sum of this centripetal acceleration plus the constant 1 Gx of Earth's gravity. This vector changes in magnitude and direction as the centrifuge rotation rate changes. Because the magnitude of the centripetal acceleration is not constant along the length of the body, this vector points increasingly footward from head to foot. Consequently, this is not a perfect simulation of the forces that would act on the body during centrifugation in microgravity. However, with respect to our hypotheses, the importance of these x-direction forces is probably negligible, because the height of the x-axis hydrostatic column is small compared with the z-axis column.
In conclusion, the heart rate data supported our hypothesis: LBNP produced the highest heart rates, followed by tilt, LAC, and SAC, which did not increase heart rate. Regional skin blood flow data were less clear, but more vasoconstriction occurred in the lower extremity during tilt and LBNP than during either form of centrifugation. These differences become potentially important when LBNP and centrifugation are considered as alternative countermeasures against the orthostatic intolerance associated with existence in microgravity. This study supports prior evidence that the peripheral vascular response to orthostatic stimulation varies significantly along the length of the body. Preservation of orthostatic vasoconstrictor capacity during long-duration spaceflight may depend on strong and repetitive simulation of gravitational pressures in the cardiovascular system. For such purposes, LBNP may be a more effective and practical means of simulating cardiovascular effects of gravity than centrifugation.
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ACKNOWLEDGMENTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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GRANTS
NASA grants 199-14-12-04 and NAG 9-1425 (to A. R. Hargens) and a National Research Council Associateship (to G. A. Breit) supported this research.
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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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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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