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Medicine & Science in Sports & Exercise:
Basic Sciences: Symposium: Physiological Adaptations and Countermeasures Associated with Long-Duration Spaceflights Restricted Physical Activity: an Update

Cardiovascular adaptation to spaceflight

HARGENS, ALAN R.; WATENPAUGH, DONALD E.

Section Editor(s): Tipton, Charles M.

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Author Information

Life Science Division (239-11), NASA Ames Research Center, Moffett Field, CA 94035-1000

Submitted for publication February 1995.

Accepted for publication December 1995.

This work was supported by NASA grant 199-14-12-04. The authors thank Karen Hutchinson, Richard Ballard, and Gita Murthy for helpful discussions and technical assistance.

Address for correspondence: Alan R. Hargens, Ph.D., Chief (Acting), Gravitational Research Branch, Life Science Division (239-11), NASA Ames Research Center, Moffett Field, CA 94035-1000.

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Abstract

This article reviews recent flight and ground-based studies of cardiovascular adaptation to spaceflight. Prominent features of microgravity exposure include loss of gravitational pressures, relatively low venous pressures, headward fluid shifts, plasma volume loss, and postflight orthostatic intolerance and reduced exercise capacity. Many of these short-term responses to microgravity extend themselves during long-duration microgravity exposure and may be explained by altered pressures (blood and tissue) and fluid balance in local tissues nourished by the cardiovascular system. In this regard, it is particularly noteworthy that tissues of the lower body (e.g., foot) are well adapted to local hypertension on Earth, whereas tissues of the upper body (e.g., head) are not as well adapted to increases in local blood pressure. For these and other reasons, countermeasures for long-duration flight should include reestablishment of higher, Earthlike blood pressures in the lower body.

Over the past 10 yr considerable progress has been made toward understanding cardiovascular adaptation to spaceflight. Although ground-based studies have been informative, in-flight experiments during the first and second dedicated Shuttle Spacelab Life Science missions (SLS-1 and SLS-2) as well as the long-duration Russian missions on the space station Mir have provided important and direct measurements during actual microgravity. Based on ground-based studies using head-down tilt (HDT) and water immersion models of microgravity as well as parabolic flight acute microgravity, investigators predicted that loss of gravitational pressure gradients and a shift of blood and tissue fluids from the legs toward the thorax would increase central venous pressure (CVP), thus initiating the expected sequence of renal and hormonal responses associated with elevation of CVP(5,44). Such responses were expected to increase urine production and reduce blood volume within the first day of microgravity exposure. However, Skylab and more recent Spacelab and Mir studies document collectively cardiac distension and a reduction of blood volume without an increase of CVP or diuresis(6,7,14,17,39). Unweighting of tissues in microgravity may reduce tissue pressures, such as intraabdominal(16) and intrathoracic pressures, in ways difficult to duplicate in ground-based simulations. Therefore, ground-based simulations of microgravity do not always accurately predict results from actual microgravity.

In this article we explore, and in some cases speculate about, the effects of long-duration exposure to microgravity on the cardiovascular system. Although Skylab and Mir missions provide the only data for periods of months in actual microgravity, the results from these missions have been presented or reviewed elsewhere(4,5,13,33,49,50,56). Thus, we primarily review and extend recent results from Spacelab missions and from our ground-based studies to provide an update to readers.

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LOSS OF GRAVITATIONALLY INDUCED BLOOD PRESSURE GRADIENTS

Exposure to microgravity undoubtedly removes the blood pressure gradients that are associated with upright posture on Earth from head to feet(Fig. 1). Thus, exposure to weightlessness reduces mean arterial pressure at the feet from about 200 mm Hg to about 100 mm Hg, the same value existent within the aorta. Also, mean arterial pressure within the head increases from a value near 70 mm Hg in upright posture on Earth to approximately 100 mm Hg in space. Therefore, blood vessels in dependent body regions are chronically exposed to lower than normal upright 1 ×g blood pressure during spaceflight, while vessels between the heart and head are exposed to higher than normal 1 × g blood pressure. Assuming that blood vessels respond appropriately to local mechanical stress conditions, one might expect that the thick-walled arteries in the feet (28,29) would experience smooth muscle atrophy while the thin-walled arteries of the head would undergo hypertrophy during extended exposure to microgravity. It is known that blood vessels respond appropriately to local stress conditions (22).

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The redistribution of blood pressures and flows in microgravity produces facial edema and volume loss from the lower extremities(49). Although the shift of blood from legs to thorax and head probably occurs within seconds, a shift of tissue fluids may occur over a period of few (2-5) hours, particularly in the legs (24,51). Within the first few hours or days of microgravity exposure, hematocrit elevation and direct measurements indicate that plasma volume decreases (SLS results;(36,37). Some plasma volume loss may precede launch because astronauts commonly experience 2 or more h in supine/legs elevated posture prior to launch. Furthermore, space motion sickness and diminished fluid intake in the first several days of microgravity exposure may contribute to plasma volume loss (39). Within 1 wk of existence in microgravity, red cell mass decreases about 10%(38,48).

When astronauts return to Earth, about half experience symptoms of orthostatic intolerance (Fig. 1), which may be due to a combination of blood volume loss, leg muscle loss, and diminished baroreflex control of blood pressure and flow to the head(5,8,9,11). Thus, blood pressure within the head may be inadequate to perfuse tissues of the brain. Crew members exposed to 1-2 wk of microgravity are sometimes orthostatically intolerant for several hours after landing. However, cosmonauts exposed to many months of microgravity sometimes require several days after return to Earth before they are able to stand and walk unaided (23). Whether there is direct correlation between the degree and duration of postflight orthostatic intolerance and duration of microgravity exposure is unknown. Upright exercise capacity is also commonly reduced postflight (13), mechanisms of this reduction are probably related to postflight orthostatic intolerance and leg muscle atrophy.

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ALTERED CEREBRAL CIRCULATION AND INTRACRANIAL PRESSURE

As previously discussed, loss of gravitational pressure in microgravity increases blood pressure to tissues of the head. In a series of studies blood and tissue fluid pressures with microgravity simulated by acute exposure to 6° HDT, we found elevated middle cerebral artery flow velocity(35) at the macrocirculatory level, increased capillary blood pressure and flow (2,45), and elevated intracranial pressure (ICP). In a recent study, ICP increased acutely from 2 mm Hg in upright posture to 17 mm Hg during 6° HDT(42). These findings suggest that the mechanism of facial, and perhaps even intracranial, edema during microgravity is increased capillary blood pressure and flow secondary to elevation of head mean arterial pressure from about 70 mm Hg in upright posture on Earth to about 100 mm Hg in space. Verification of this theory awaits studies of blood pressure and flow as well as ICP during microgravity. Based on ground studies to date, capillary pressures should also equalize at approximately 30 mm Hg through the body(Fig. 2). Besides increased capillary pressure and flow during HDT, an early decrease of plasma colloid osmotic pressure due to net reabsorption of interstitial fluid from lower body tissues(24) also promotes edema formation in tissues of the head(45). Taken together, these pressure and flow factors may be responsible for the facial edema that appears in some astronauts and cosmonauts during their mission. Furthermore, the elevation of headward blood pressure and flow as well as ICP may be initiating factors for the early space motion sickness (26,52), reduction of fluid intake/negative fluid balance, and later headward redistribution of bone(3; Schneider, this symposium).

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MICROCIRCULATORY ADAPTATION TO GRAVITY

Because the feet and head experience the greatest change in blood pressure during microgravity, it is worth-while to understand their structure and functional responses to gravitational stimuli. Recently we found that elevation of blood pressure to the head produced by transition from 60° head-up tilt (HUT) to 6° HDT (Fig. 3) increases microcirculatory blood flow in skin of the head (2). This pressure and flow increase may be expected in a tissue not commonly exposed to increased blood pressure and therefore not able to regulate blood flow closely and prevent edema. On the other hand, moving the body from 6° HDT to 60° HUT actually reduces microcirculatory flow in the foot. This response suggests that the microcirculation of the lower body, normally adapted to upright posture on Earth, is able to regulate capillary pressure and flow well to prevent dependent edema (32,47). In combination with a thicker capillary basement membrane in dependent tissues(57) to reduce hydraulic conductivity, other mechanisms for preventing dependent edema include lymphatic drainage(25), the venoarteriolar reflex(32), and venous pumps in the leg(47).

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MYOCARDIAL FUNCTION AND BAROREFLEX CONTROL IN MICROGRAVITY

Although rat studies on recent Cosmos flights indicate myocardial degeneration during 2-wk exposure to microgravity (46), Russian investigators believe the human heart is well protected during long-duration exposure to microgravity (4), except for a loss of chamber volume to levels seen while upright on Earth(11). However, magnetic resonance imaging results from the D-2 Spacelab flight suggest reduction of myocardial mass (C. G. Blomqvist, personal communication). Chronically reduced preload (cardiac filling pressure) in microgravity(6,7,17,36,37) appears to reduce chamber volume (11), whereas relatively constant afterload (arterial blood pressure) prevents loss of cardiac contractile function or wall thickness (33,41).

Lack of gravitational (postural) stimulation in microgravity may reduce baroreflex sensitivity. Evidence for a compromised vascular arm of baroreflexes is mixed: one study reported reduced elevation of total peripheral resistance (TPR) upon standing postflight(41), while another noted a tendency for the TPR response to lower-body negative pressure (LBNP) to be increased postflight(19,20). Buckey and coworkers(8) found that astronauts who could not complete a 10-min stand test after spaceflight exhibited a blunted increase in TPR upon standing relative to preflight measurements, whereas astronauts who tolerated the entire 10 min of standing postflight exhibited an accentuated TPR response to standing relative to preflight and to the nonfinishers. It should be noted that a “normal” (preflight) level of orthostatic vasoconstriction observed postflight in spite of the additional cardiovascular stress imposed by hypovolemia would indicate inadequate function of the vascular baroreflex arm. The mechanism of vascular baroreflex dysfunction in subjects prone to fainting after spaceflight (vascular smooth muscle atrophy neurovascular hyporesponsiveness, or baroreflex resetting?) requires further study.

Some evidence suggests that microgravity desensitizes the cardiac arm of the carotid baroreflex: the change in R-R interval for a given change in arterial pressure is commonly reduced after spaceflight(21). However, Rowell (47) questions baroreflex assessments based on R-R interval changes, in part because they ignore the contribution of stroke volume to cardiac output. For example, heart rate increases more during in-flight LBNP than during preflight LBNP(12,34), and standing heart rate is elevated postflight (11) to compensate for the stroke volume deficit imposed by microgravity-induced hypovolemia (8). These observations alone imply adequate function of the cardiac baroreflex arm.

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COUNTERMEASURES FOR THE CARDIOVASCULAR SYSTEM

Presently, countermeasures for short-duration Shuttle flights focus on prevention of postflight orthostatic intolerance. For this reason, a countermeasure using 4 h of LBNP at 30 mm Hg along with 1 quart of water and eight salt tablets (effectively about 1 1 of isotonic saline) has been used to attempt to maintain adequate blood pressure and flow to the head during and immediately after landing the Shuttle(10,12,18). Use of fluid loading alone is more common, yet only partially effective (8,9): seven of 12 Shuttle crew members who ingested saline in-flight could not stand for 10 min on landing day (8). Shuttle astronauts routinely wear anti-G suits during return to Earth from orbit. Other recently proposed countermeasures for short-duration flights include a single maximal bout of exercise within 1 d of landing (15) and administration of fludrocortisone to raise plasma volume(53).

Although exercise had been considered one of the primary strategies for maintaining cardiovascular and aerobic fitness during long-duration flight, it is apparent that no hardware presently planned for Shuttle or Space Station is able to provide the static and inertial pressure gradients existent on Earth within the arteries and veins of the lower body. Therefore, we have proposed use of treadmill exercise within LBNP (Fig. 4) to provide musculoskeletal stresses similar to gravity (31) as well as Earth-like transmural pressures across blood vessels of the lower body during long-duration spaceflight (27,30). Recent experiments confirm that supine exercise during LBNP effectively reproduces many musculoskeletal (Fig. 5) and cardiovascular stresses of upright exercise in 1 × g(27,43,54,55). Normally, sustained high levels of LBNP lead to syncope, but exercise alone may be sufficient to maintain adequate cerebral perfusion during LBNP (55). Other potential problems with this counter-measure include herniae during LBNP exercise and cephalad fluid shifts after LBNP release.

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Future directions for microgravity-related cardiovascular research were reviewed in September 1995 at the International Workshop on Cardiovascular Research in Space. The proceedings of that workshop will be presented inMedicine and Science in Sports and Exercise this year.

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HUMAN; MICROGRAVITY; WEIGHTLESSNESS; GRAVITATIONAL BLOOD PRESSURES; MICROCIRCULATION; COUNTERMEASURES

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Shimoyama, R; Miyata, H; Ohama, E; Kawai, Y
Japanese Journal of Physiology, 50(1): 141-147.

Journal of Applied Physiology
Vascular adaptation to microgravity: what have we learned?
Zhang, LF
Journal of Applied Physiology, 91(6): 2415-2430.

Journal of Biomechanics
Reduced oxygen release from erythrocytes by the acceleration-induced flow shift, observed in an oxygen-permeable narrow tube
Tateishi, N; Suzuki, Y; Shirai, M; Cicha, I; Maeda, N
Journal of Biomechanics, 35(9): 1241-1251.
PII S0021-9290(02)00068-4
CrossRef
Hippokratia
The therapeutic benefits of gravity in space and on earth
Kourtidou-Papadeli, C; Papadelis, CL; Vernikos, J; Pd, B; Hitoglou-Antoniadou, M; Perantoni, E; Vlachogiannis, E
Hippokratia, 12(): 28-31.

Aviation Space and Environmental Medicine
Decongestant effects on hemodynamics at rest, exercise, and recovery from exercise during -6 degrees of head down tilt
Rosene, JM; Rosene, JA; Koczajowski, DL; Paolone, VJ
Aviation Space and Environmental Medicine, 70(1): 15-21.

Journal of Applied Physiology
Blood pressure and mesenteric resistance arterial function after spaceflight
Hatton, DC; Yue, Q; Chapman, J; Xue, H; Dierickx, J; Roullet, C; Coste, S; Roullet, JB; McCarron, DA
Journal of Applied Physiology, 92(1): 13-17.

Acta Physiologica Scandinavica
Proposed role of the paraventricular nucleus in cardiovascular deconditioning
Mueller, PJ; Cunningham, JT; Patel, KP; Hasser, EM
Acta Physiologica Scandinavica, 177(1): 27-35.

Journal of Applied Physiology
Effect of microgravity on the expression of mitochondrial enzymes in rat cardiac and skeletal muscles
Connor, MK; Hood, DA
Journal of Applied Physiology, 84(2): 593-598.

Japanese Circulation Journal-English Edition
Successful treatment of malignant neurocardiogenic syncope with repeated tilt training program
Numata, T; Abe, H; Nagatomo, T; Sonoda, S; Kohshi, K; Nakashima, Y
Japanese Circulation Journal-English Edition, 64(5): 406-409.

Behavioural Brain Research
Simulated weightlessness aggravates hypergravity-induced impairment of learning and memory and neuronal apoptosis in rats
Sun, XQ; Xu, ZP; Zhang, S; Cao, XS; Liu, TS
Behavioural Brain Research, 199(2): 197-202.
10.1016/j.bbr.2008.11.035
CrossRef
American Journal of Physiology-Cell Physiology
Activation of BKCa channel is associated with increased apoptosis of cerebrovascular smooth muscle cells in simulated microgravity rats
Xie, MJ; Ma, YG; Gao, F; Bai, YG; Cheng, JH; Chang, YM; Yu, ZB; Ma, J
American Journal of Physiology-Cell Physiology, 298(6): C1489-C1500.
10.1152/ajpcell.00474.2009
CrossRef
Aviation Space and Environmental Medicine
Medical imaging in microgravity
Jadvar, H
Aviation Space and Environmental Medicine, 71(6): 640-646.

Aviation Space and Environmental Medicine
Angiotensinogen and AT1R expression in cerebral and femoral arteries during hindlimb unloading in rats
Bao, JX; Zhang, LF; Ma, J
Aviation Space and Environmental Medicine, 78(9): 852-858.

Journal of Applied Physiology
Autonomic cardiovascular and respiratory control during prolonged spaceflights aboard the International Space Station
Baevsky, RM; Baranov, VM; Funtova, II; Diedrich, A; Pashenko, AV; Chernikova, AG; Drescher, J; Jordan, J; Tank, J
Journal of Applied Physiology, 103(1): 156-161.
10.1152/japplphysiol.00137.2007
CrossRef
Acta Physiologica Hungarica
Regional specificity of adaptation change in large elastic arteries of simulated microgravity rats
Gao, F; Bao, JX; Xue, JH; Huang, J; Huang, WQ; Wu, SX; Zhang, LF
Acta Physiologica Hungarica, 96(2): 167-187.
10.1556/APhysiol.96.2009.2.3
CrossRef
Hormone and Metabolic Research
Effect of simulated microgravity on endocrine response to insulin-induced hypoglycemia in physically fit men
Ksinantova, L; Koska, J; Kvetnansky, R; Marko, M; Hamar, D; Vigas, M
Hormone and Metabolic Research, 34(3): 155-159.

Journal of Applied Physiology
Simulated microgravity enhances vasoconstrictor responsiveness of rat basilar artery
Zhang, LN; Zhang, LF; Ma, J
Journal of Applied Physiology, 90(6): 2296-2305.

American Journal of Physiology-Heart and Circulatory Physiology
Hypovolemia and neurovascular control during orthostatic stress
Kimmerly, DS; Shoemaker, JK
American Journal of Physiology-Heart and Circulatory Physiology, 282(2): H645-H655.

Aviation Space and Environmental Medicine
Anesthesia during and after exposure to microgravity
Agnew, JW; Fibuch, EE; Hubbard, JD
Aviation Space and Environmental Medicine, 75(7): 571-580.

Clinical Science
Chronic fatigue syndrome: comments on deconditioning, blood volume and resulting cardiac function
Stewart, JM
Clinical Science, 118(): 121-123.
10.1042/CS20090327
CrossRef
Journal of Cellular Biochemistry
Clinorotation Upregulates Inducible Nitric Oxide Synthase by Inhibiting AP-1 Activation in Human Umbilical Vein Endothelial Cells
Wang, YC; Zhang, S; Du, TY; Wang, B; Sun, XQ
Journal of Cellular Biochemistry, 107(2): 357-363.
10.1002/jcb.22134
CrossRef
Journal of Applied Physiology
Simulated microgravity increases myogenic tone in rat cerebral arteries
Geary, GG; Krause, DN; Purdy, RE; Duckles, SP
Journal of Applied Physiology, 85(5): 1615-1621.

Journal of Applied Physiology
Hindlimb unweighting induces changes in the p38(MAPK) contractile pathway of the rat abdominal aorta
Summers, SM; Hayashi, Y; Nguyen, SV; Nguyen, TM; Purdy, RE
Journal of Applied Physiology, 107(1): 121-127.
10.1152/japplphysiol.00210.2009
CrossRef
Ultrasound in Medicine and Biology
Ultrasound Evaluation of Site-Specific Effect of Simulated Microgravity on Articular Cartilage
Wang, Q; Zheng, YP; Wang, XY; Huang, YP; Liu, MQ; Wang, SZ; Zhang, ZK; Guo, X
Ultrasound in Medicine and Biology, 36(7): 1089-1097.
10.1016/j.ultrasmedbio.2010.04.018
CrossRef
Aviation Space and Environmental Medicine
Quantitative phase contrast images to quantitate flow in a rat model of microgravity
Hays, AM; Keller, RL; Gmitro, AF; Alpbach, MI; Sridhar, KR; Balagtas, MP; Witten, ML
Aviation Space and Environmental Medicine, 70(3): 225-229.

Biomedizinische Technik
Polygraphic belt with force-sensing expander for physiological tests on cosmonauts
Rafolt, D; Gallasch, E
Biomedizinische Technik, 46(9): 230-235.

Adaptation Biology and Medicine, Vol 3: New Frontiers
Structural and functional adaptations of vessels to microgravity
Zhang, LF; Zhang, LN
Adaptation Biology and Medicine, Vol 3: New Frontiers, (): 179-190.

Journal of Applied Physiology
Effectiveness of intermittent -G(x) gravitation in preventing deconditioning due to simulated microgravity
Zhang, LF; Sun, B; Cao, XS; Liu, C; Yu, ZB; Zhang, LN; Cheng, JH; Wu, YH; Wu, XY
Journal of Applied Physiology, 95(1): 207-218.
10.1152/japplphysiol.00969.2002
CrossRef
Europace
Repeated tilt testing in patients with tilt-positive neurally mediated syncope
Ector, H; Willems, R; Heidbuchel, H; Reybrouck, T
Europace, 7(6): 628-633.
10.1016/j.eupc.2005.06.011
CrossRef
Spine
Effects of reloading after simulated microgravity on proteoglycan metabolism in the nucleus pulposus and anulus fibrosus of the lumbar intervertebral disc
Yasuoka, H; Asazuma, T; Nakanishi, K; Yoshihara, Y; Sugihara, A; Tomiya, M; Okabayashi, T; Nemoto, K
Spine, 32(): E734-E740.

Aviation Space and Environmental Medicine
Peripheral effector mechanism hypothesis of postflight cardiovascular dysfunction
Zhang, LF; Yu, ZB; Ma, J; Mao, QW
Aviation Space and Environmental Medicine, 72(6): 567-575.

Journal of Applied Physiology
Daily short-period gravitation can prevent functional and structural changes in arteries of simulated microgravity rats
Sun, B; Zhang, LF; Gao, F; Ma, XW; Zhang, ML; Liu, J; Zhang, LN; Ma, J
Journal of Applied Physiology, 97(3): 1022-1031.
10.1152/japplphysiol.00188.2004
CrossRef
American Journal of Physiology-Heart and Circulatory Physiology
Functional alterations in cerebrovascular K+ and Ca2+ channels are comparable between simulated microgravity rat and SHR
Xie, MJ; Zhang, LF; Ma, J; Cheng, HW
American Journal of Physiology-Heart and Circulatory Physiology, 289(3): H1265-H1276.
10.1152/ajpheart.00074.2005
CrossRef
Vascular Pharmacology
Hindlimb unweighting induces changes in the RhoA-Rho-kinase pathway of the rat abdominal aorta
Summers, SM; Nguyen, SV; Purdy, RE
Vascular Pharmacology, 48(): 208-214.
10.1016/j.vph.2008.03.006
CrossRef
Aviation Space and Environmental Medicine
Aerobic Exercise Deconditioning and Countermeasures During Bed Rest
Lee, SMC; Moore, AD; Everett, ME; Stenger, MB; Platts, SH
Aviation Space and Environmental Medicine, 81(1): 52-63.
10.3357/ASEM.2474.2010
CrossRef
American Journal of Physiology-Regulatory Integrative and Comparative Physiology
Hindlimb unloading alters nitric oxide and autonomic control of resting arterial pressure in conscious rats
Mueller, PJ; Foley, CM; Hasser, EM
American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 289(1): R140-R147.
10.1152/ajpregu.00820.2004
CrossRef
Current Pharmaceutical Biotechnology
Benefit of repeated receptor stimulation as a spaceflight medical tool to promote cardiovascular fitness: Different orthostatic paradigms compared
Hinghofer-Szalkay, H; Rossler, A
Current Pharmaceutical Biotechnology, 6(4): 253-266.

Japanese Journal of Physiology
Contractile responses of the basilar artery isolated from rabbits exposed to 8-day head-down tilt
Ueda, K; Aoyama, Y; Sasaka-Kitamura, F; Kawai, Y
Japanese Journal of Physiology, 51(2): 209-215.

Medicine & Science in Sports & Exercise
Neuroendocrine and immune system responses with spaceflights
TIPTON, CM; GREENLEAF, JE; JACKSON, CG
Medicine & Science in Sports & Exercise, 28(8): 988-998.

Medicine & Science in Sports & Exercise
Lower-body negative-pressure exercise and bed-rest–mediated orthostatic intolerance
SCHNEIDER, SM; WATENPAUGH, DE; LEE, SM; ERTL, AC; JON WILLIAMS, W; BALLARD, RE; HARGENS, AR
Medicine & Science in Sports & Exercise, 34(9): 1446-1453.

PDF (1092)
The American Journal of the Medical Sciences
Plasma and Blood Volume in Space
Diedrich, A; Paranjape, SY; Robertson, D
The American Journal of the Medical Sciences, 334(1): 80-85.
10.1097/MAJ.0b013e318065b89b
PDF (543) | CrossRef
Journal of Trauma and Acute Care Surgery
Extraterrestrial Resuscitation of Hemorrhagic Shock: Fluids
Hamilton, DR; Dawson, DL; Williams, DR; Kirkpatrick, AW; Dulchavsky, SA; Boulanger, BR; Campbell, MR
Journal of Trauma and Acute Care Surgery, 50(1): 162-168.

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