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J Appl Physiol 103: 156-161, 2007. First published April 19, 2007; doi:10.1152/japplphysiol.00137.2007
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Autonomic cardiovascular and respiratory control during prolonged spaceflights aboard the International Space Station

Roman M. Baevsky,1 Victor M. Baranov,1 Irina I. Funtova,1 André Diedrich,3 Andrey V. Pashenko,1 Anja G. Chernikova,1 Jürgen Drescher,4 Jens Jordan,2 and Jens Tank2

1Institute of Biomedical Problems, Moscow, Russia; 2Medical Faculty of the Charité, Franz Volhard Clinic, Helios Clinic, Berlin, Germany; 3Department of Medicine, Division of Clinical Pharmacology, Autonomic Dysfunction Center, Vanderbilt University School of Medicine, Nashville, Tennessee; and 4German Aerospace Center, Cologne, Germany

Submitted 1 February 2007 ; accepted in final form 9 April 2007


   ABSTRACT
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 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
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Impaired autonomic control represents a cardiovascular risk factor during long-term spaceflight. Little has been reported on blood pressure (BP), heart rate (HR), and heart rate variability (HRV) during and after prolonged spaceflight. We tested the hypothesis that cardiovascular control remains stable during prolonged spaceflight. Electrocardiography, photoplethysmography, and respiratory frequency (RF) were assessed in eight male cosmonauts (age 41–50 yr, body-mass index of 22–28 kg/m2) during long-term missions (flight lengths of 162–196 days). Recordings were made 60 and 30 days before the flight, every 4 wk during flight, and on days 3 and 6 postflight during spontaneous and controlled respiration. Orthostatic testing was performed pre- and postflight. RF and BP decreased during spaceflight (P < 0.05). Mean HR and HRV in the low- and high-frequency bands did not change during spaceflight. However, the individual responses were different and correlated with preflight values. Pulse-wave transit time decreased during spaceflight (P < 0.05). HRV reached during controlled respiration (6 breaths/min) decreased in six and increased in one cosmonaut during flight. The most pronounced changes in HR, BP, and HRV occurred after landing. The decreases in BP and RF combined with stable HR and HRV during flight suggest functional adaptation rather than pathological changes. Pulse-wave transit time shortening in our study is surprising and may reflect cardiac output redistribution in space. The decrease in HRV during controlled respiration (6 breaths/min) indicates reduced parasympathetic reserve, which may contribute to postflight disturbances.

autonomic nervous system; microgravity; spaceflight; heart rate variability; cardiovascular physiology

THE LACK OF GRAVITATIONAL stress during prolonged spaceflights is associated with adaptation in cardiovascular structure and neurohumoral control circuits (22, 36, 41, 42). These alterations could increase cardiac arrhythmias and diminish the ability of the cardiovascular system to cope with gravitational stress after returning to Earth (36, 41). Together with loss of bone and skeletal muscle mass, cardiovascular maladaptation could conceivably limit the duration of space travel. Moreover, the effects of long-term spaceflight on blood pressure (BP) as a subsequent risk factor are unknown. However, a recent analysis challenges the concept that spaceflights are "unhealthy" for the cardiovascular system (30). Experimental evidence suggesting increased risk for cardiac disease during prolonged spaceflights is lacking (8). The current concepts regarding cardiovascular adaptation in space may be biased by the large number of short-term studies (42). Published data on long-term flights, which could have relevance on the recently touted plans to visit Mars, are rare. Even data on simple measurements such as heart rate (HR), BP, respiratory frequency (RF), or heart rate variability (HRV) are conflicting (10, 17, 18, 29, 30, 40). Furthermore, cardiovascular deconditioning was not a major scientific health issue during the long-term missions aboard the Russian MIR (25). Early results from animal experiments on Russian space satellites II–V and from the first cosmonauts Gagarin and Titov provide no long-term insight into cardiovascular regulation (32). In addition, results from the International Space Station (ISS) reported earlier that were based on 24-h recordings are confounded with physical countermeasure routines or the work schedule (18, 19). We tested the hypothesis that cardiovascular control remains stable during prolonged spaceflight aboard the ISS.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Subjects.   We studied eight male cosmonauts during space missions aboard the ISS (age 41–50 yr, height 1.74–1.82 m, weight 70–90 kg). The duration of the missions varied between 162 and 196 days. A 24-h daily schedule with alternating sleep-wake and work cycles was maintained during the flight. The daily routine included time for exercise for up to 2 h. Three exercise days were followed by 1 day without exercise. All cosmonauts had extravehicular activities during the flight. The Committee for Research Policies and Procedures of the Institute for Biomedical Problems (Moscow, Russia) approved the protocol, which followed all guidelines stated in the Helsinki accords.

Protocol.   Cosmonauts were carefully trained to perform the in-flight measurements by themselves. Measurements were obtained 60 and 30 days before the flight, approximately monthly during flight, and on days 3 and 6 after return to Earth. Subjects rested for at least 30 min before measurements were started. Periods of 10 min of spontaneous respiration and 3 min of controlled respiration following a timer at 12 and 6 breaths/min were recorded. Orthostatic testing (10 min supine, 10 min upright) was performed during pre- and postflight measurements. Cosmonauts were in a semi-supine position during controlled respiration to follow the instructions on the laptop screen. Ambient conditions on the ground were comparable to the conditions aboard the ISS. Measurements were performed at least 2 h after the last food or fluid intake and preceded physical exercise or work tasks.

Data acquisition and analysis.   The hardware-software diagnostic complex "Pulse" (Fig. 1) was used during pre-, in-, and postflight experiments. ECG, photoplethysmography, and respiration were recorded at 1-kHz sample rate (Fig. 1); results were saved on memory cards for off-line analysis on Earth. HR, RF, and HRV in the time and frequency domain were analyzed. Brachial BP was measured by use of the onboard oscillometric device (TensoPlus). The pulse-wave transit time (PWTT) was determined as time interval between the R peak in the ECG and the onset of the photo pulse wave at the finger tip. The software "Orbit" was used, which consists of the data-acquisition system, display of the biosignals, and the instructions guiding the cosmonaut throughout the tests.


Figure 1
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  		Fig. 1. The "Pulse" device (top left), 1 cosmonaut during the experiment aboard the International Space Station (top right), and a representative tracing of data recorded during controlled respiration (12 breaths/min) (bottom). PPG, photoplethysmogram; Resp, respiration.

 
Spectral analysis.   HRV was determined by spectral analysis (1, 39). Briefly, beat-to-beat series were interpolated and resampled at 4 Hz. The power spectra density was estimated by the Welsh method with zero padding, linear trend elimination, and a 50% overlapped Hanning window. Low-frequency (LF) power (0.04–0.15 Hz), high-frequency (HF) power (0.15–0.4 Hz), and the LF-to-HF ratio (LF/HF) were calculated. HF power reflects mainly parasympathetic HR control. LF power reflects both sympathetic and parasympathetic HR control. The LF/HF has been suggested by some investigators to reflect sympathovagal balance of HR control (1, 13, 31).

Statistics.   Data are expressed as means ± SE. One-way ANOVA for repeated measures was used to test for differences. The posttest was computed only if the overall P was <0.05. We relied on the Bonferroni post hoc test. Differences between preflight and in-flight values after 5 mo in space were compared by the nonparametric Wilcoxon matched-pairs test. Linear regression analysis was used if indicated. A value for P < 0.05 was considered significant.


   RESULTS
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DISCUSSION
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All data sets obtained in space were of good quality, with <2% artifacts in the records. Preflight (–60 and –30 days) recordings of one cosmonaut could not be analyzed completely because of artifacts in the ECG signal. Thus the Pulse device, combined with Orbit software, was suitable for self-guided experiments in space. BP and RF decreased during spaceflight. Comparisons between individual preflight values and values obtained after 5 mo in space showed significant differences (Fig. 2; P < 0.05). RF decreased to values close to 6 breaths/min (i.e., 0.1 Hz) in some cosmonauts. Mean HR did not change during spaceflight. The individual changes in HR after 5 mo in space were correlated with preflight supine values (r2 = 0.572, P < 0.05). Figure 3 shows the mean values of HR, RF, and BP before, during, and after spaceflight.


Figure 2
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  		Fig. 2. Individual values of heart rate (HR; top left), respiratory frequency (RF; top right), systolic blood pressure (SBP; bottom left), and diastolic blood pressure (DBP; bottom right) before flight (preflight) compared with individual values after 5 mo in space (M5); n = 8 subjects. P < 0.05 (Wilcoxon matched pairs test).

 

Figure 3
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  		Fig. 3. Mean values ± SE of HR (top), SBP ({blacktriangledown}) and DBP ({blacktriangleup}) (middle), and RF (bottom) 60 and 30 days before the flight (–60, –30), during flight (monthly measurements, M01–M06), and 3 and 6 days after landing (+3, +6). The preflight and postflight values are supine measurements. bpm, Beats/min. *P < 0.05 (one-way ANOVA for repeated measures compared with preflight values).

 
PWTT, which is thought to be negatively correlated with arterial BP, was shorter in space and decreased further after spaceflight (Fig. 4). Return to Earth rapidly reversed the changes for BP, HR, and RF but not for PWTT. Indeed, BP, HR, and RF after return to Earth exceeded the baseline values before spaceflight. Power spectral densities in the LF and the HF band and the LF/HF did not change significantly during spaceflight (Fig. 5). The large interindividual differences are in accordance with the results from other studies. After the cosmonauts had landed, HF power of HRV was shown to be decreased compared with preflight values. However, our study does not have the statistical power to identify a subtle change in HRV. LF power, HF power, and the LF/HF differed dramatically between controlled respiration at a frequency of 12 breaths/min and spontaneous breathing. The RF of ~6 breaths/min in some cosmonauts explains the high LF-power values during spontaneous respiration and the tendency of an increased LF/HF. HRV was not decreased in space in our study.


Figure 4
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  		Fig. 4. Left: mean values ± SE of pulse-wave transit time (PWTT; in ms) 60 and 30 days before the flight, during flight (monthly measurements), and 3 and 6 days after landing. *P < 0.05 (one-way ANOVA for repeated measures compared with preflight values). Right: individual values of PWTT before flight compared with individual values after 5 mo in space (M5); n = 8 subjects. P < 0.05 (Wilcoxon matched pairs test).

 

Figure 5
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  		Fig. 5. Mean values ± SE of absolute HR variability data in the low-frequency (LF-RR) and high-frequency (HF-RR) bands and the LF/HF ratio (LF/HF-RR) during controlled respiration (CR 12 breaths/min) compared with spontaneous respiration (SR) at 60 and 30 days before the flight, during flight (monthly measurements), and 3 and 6 days after landing. *P < 0.05 (one-way ANOVA for repeated measures compared with preflight values).

 
Controlled respiration in the LF range (6 breaths/min) profoundly increases HRV power to an individual maximum (23) in normal subjects by concentrating and augmenting the HRV power in the LF band. Therefore, the HRV power, calculated as mean value in the LF range during controlled respiration at 6 breaths/min, reflects individual parasympathetic capacity. Despite large interindividual differences, LF power of HRV attained during controlled respiration at 6 breaths/min decreased during flight in six cosmonauts and increased in one cosmonaut (Fig. 6). Total power of HRV during spontaneous respiration did not decrease during flight (preflight: 1,918 ± 728 ms2, after 5 mo in space: 1,847 ± 473 ms2, not significant) and remained lower than HRV power attained during controlled respiration at 6 breaths/min.


Figure 6
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  		Fig. 6. Left: mean values ± SE of absolute HR variability power in the RF range (power at RF) during controlled respiration at 6 breaths/min (CR 6/min) 60 and 30 days before the flight, during flight (monthly measurements), and 3 and 6 days after landing. Right: individual values of HR variability power in the RF range during controlled respiration at 6 breaths/min before flight compared with individual values after 5 mo in space (M5); n = 7 subjects. P < 0.05 (Wilcoxon matched pairs test). ns, Not significant.

 
The mean HR change with standing was 12 ± 1 beats/min on preflight day 60, 14 ± 2 beats/min on preflight day 30, 21 ± 2 beats/min on postflight day 3, and 21 ± 2 beats/min on postflight day 6 (not significant between days). Only one cosmonaut (cosmonaut 1) exhibited a greater HR increase than 30 beats/min (31 beats/min), which is the diagnostic cut-off value for diagnosing postural orthostatic tachycardia (2). He declined to undergo orthostatic testing on postflight day 6. He showed the highest HF power of HRV during controlled breathing (12 breaths/min) in-flight, the most pronounced increase in BP postflight, and high-preflight HR.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
We studied eight Russian cosmonauts before, during, and after a long-term space mission aboard the ISS. The main findings of our study were that BP and RF decreased in space, whereas mean HR and HRV did not change. However, the maximum respiratory sinus arrhythmia reached during controlled respiration at RF of 6 breaths/min decreased in six of seven cosmonauts during flight and did not reach preflight values after return to Earth. Sustained orthostatic intolerance after return to Earth was uncommon. Previous studies were conducted during short-term spaceflights (18, 21, 29), relied on 24-h Holter monitoring (18, 19), did not control for RF (18, 19, 21), or were limited by the small sample size (10, 38).

Differences between earlier studies and our study may be explained by different mechanisms involved in acute and chronic adaptation to spaceflight (21, 22, 38, 42). Initially, microgravity causes acute fluid shifts toward the upper parts of the body. Many cosmonauts describe flu-like symptoms, including headache, swelling of the head ("puffy faces"), and nasal congestion (20). Remarkably, central venous pressure decreases (5). The acute phase is accompanied by motion sickness (24) and increased sympathetic activity (7, 14, 17). Chronically, plasma volume and red cell mass decrease with normalization in interstitial volumes (5, 6, 9, 12, 17, 26, 28). Left ventricular mass decreases 12% over 10 days in space (33). We obtained our first measurements after 1 mo in space when all acute symptoms had already abated. Our results are giving insight in chronic cardiovascular and respiratory adaptation to microgravity.

We observed a depressor response in space while HR remained stable. In contrast, after 120 and 180 days in space, Cooke et al. (10) observed HR reduction in one of two cosmonauts. Diastolic BP decreased in both cosmonauts reported in that study. In another long-term observation, HR and diastolic BP decreased (18). Polysomnography testing showed HR reduction both while subjects were awake and during all sleep stages (21). Mean HR obtained over periods of up to 24 h did not vary over the course of a long-term mission (19). HR was found to be reduced by 9 beats/min compared with preflight standing values but above supine preflight values during prolonged spaceflights (35). Thus most studies suggest that long-term exposure to microgravity decreases BP. HR responses in space appear to depend on preflight values (21) and differ interindividually.

The depressor response may result from vasodilatation in space because cardiac output tends to increase (30) and cardiac contractility remains stable (3). Therefore, PWTT shortening in our study is surprising. The observation suggests increased rather than decreased peripheral vascular tone. Furthermore, an earlier study showed increased calf vascular resistance during short-term spaceflight (40). One possible explanation for the discrepancy is cardiac output redistribution in space. Differential resistance vessel remodeling may be involved (43).

RF reduction has not been previously shown in space. Lung volumes were found to be reduced during short-term spaceflight (16). Tidal volume, pulmonary ventilation, and metabolic rate were found to be reduced compared with preflight standing measures (35). Vital capacity and respiratory muscle strength are maintained during long-term spaceflight (34). It is possible that RF reduction is not compensated for by increased tidal volume, which could be a physiological response to reduced metabolic demand (21, 34, 37).

One important implication of our study is that HRV data in space cannot be interpreted in the absence of RF measurements or controlled respiration experiments. The difference in HRV between controlled and spontaneous breathing increased dramatically in space and was mainly related to the reduced RF in space. The trend of increased LF/HF in space during spontaneous breathing was reversed during controlled breathing at 12 breaths/min. With short-term exposure to simulated or real microgravity, HRV (10, 18, 19) and baroreflex sensitivity (10, 15) decreased in several studies. In others, HRV was similar to preflight values (21, 29). HRV reduction in some studies may be secondary to acute physiological and psychological stress exerted during early phases of spaceflight. Our study suggests that resting autonomic HR control remains relatively stable with chronic microgravity. Numerically, mean resting HRV even increased in space, which may be explained by increased parasympathetic or decreased sympathetic HR control at least in some cosmonauts. However, interindividual differences were large and depended on preflight HR control. Respiratory sinus arrhythmia is primarily mediated through the parasympathetic nervous system. HRV reduction during controlled respiration at RF of 6 breaths/min may indicate reduced parasympathetic capacity or reserve (27). Attenuated functional reserve during spaceflight exceeding an individual threshold may perhaps predispose to complications after return to Earth (4).

One of eight cosmonauts experienced orthostatic intolerance 3 days after flight. Sympathetic baroreflex regulation, {alpha}1-adrenoreceptor responsiveness, and tyramine-evoked norepinephrine release appear to be altered in astronauts prone to experiencing orthostatic symptoms after return to Earth (28). Whether reduced parasympathetic reserve is involved in postflight orthostatic intolerance deserves further study.

Measurements on the ISS are difficult. The cosmonauts have a busy schedule and reside in cramped quarters. Therefore, our study has limitations. The controlled breathing tests on Earth were not obtained in a perfectly supine position, which may have influenced our results. We did not control tidal volume during spaceflight. However, it has been shown that it is not necessary to control inspired volumes during identical controlled-frequency breathing protocols (11). We have not been able to obtain longer-term follow-up in our subjects. We also cannot comment on long-term cardiovascular risk engendered by prolonged spaceflight on the basis of these data.

Perspectives.   Trained cosmonauts are able to perform simple autonomic cardiovascular tests during spaceflight. These tests may have utility in guiding personal training and work time schedules. The observed decreases in RF and BP may support the provocative hypothesis that flying in space is healthy for the human cardiovascular system (30). Moreover, our results indicate that the cardiovascular training program aboard the ISS was sufficient to prevent substantial cardiovascular symptoms after return to Earth. Elucidation of mechanisms responsible for the remodeling of the central nervous system circuits involved in respiratory and cardiovascular control may help to define new treatments for the prevention of in-flight and postflight disturbances.


   GRANTS
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 ABSTRACT
 METHODS
 RESULTS
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 GRANTS
REFERENCES
 
This work was supported by grants from the Bundesministerium fuer Bildung und Forschung and the German Aerospace Center.


   FOOTNOTES
 

Address for reprint requests and other correspondence: J. Tank, Franz-Volhard Clinical Research Center, Haus 129, Wiltbergstr. 50, 13125 Berlin, Germany (e-mail: jens.tank{at}charite.de)

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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