1 Department of Surgery, University of Medicine and Dentistry of New Jersey-School of Osteopathic Medicine, Stratford, New Jersey 08084; and 2 Life Sciences Division, National Aeronautics and Space Administration-Ames Research Center, Moffett Field, California 94035
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Compared with men, women appear to have a decreased sympathetic nervous system (SNS) response to stress. The two manifestations where the sexual dimorphism has been the most pronounced involve the response of the SNS to fluid shifts and fuel metabolism during exercise. The objectives of this study were to investigate whether a similar sexual dimorphism was found in the response to spaceflight. To do so, we compared catecholamine excretion by male and female astronauts from two similar shuttle missions, Spacelab Life Sciences 1 (SLS1, 1991) and 2 (SLS2, 1993) for evidence of sexual dimorphism. To evaluate the variability of the catecholamine response in men, we compared catecholamine excretion from the two SLS missions against the 1996 Life and Microgravity Sciences Mission (LMS) and the 1973 Skylab missions. Results: No gender- or mission-dependent changes were found with epinephrine. Separating out the SLS1/2 data by gender shows that norepinephrine excretion was essentially unchanged with spaceflight in women (98 ± 10%; n = 3) and substantially decreased with the men (41 ± 9%; n = 4, P < 0.05). Data are a percentage of mean preflight value ± SE. Comparisons among males demonstrated significant mission effects on norepinephrine excretion. After flight, there was a transient increase in norepinephrine but no evidence of any gender-specific effects. We conclude that norepinephrine excretion during spaceflight is both mission and gender dependent. Men show the greater response, with at least three factors being involved, a response to microgravity, energy balance, and the ratio of carbohydrate to fat in the diet.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
ALTHOUGH THE MAJORITY OF ASTRONAUTS are men, the proportion of female astronauts is increasing. Future missions, including long-duration missions on the space station and eventually to Mars, are expected to include both men and women. Yet few studies have addressed the question of whether there are gender differences in the responses to spaceflight. There may well be. In recent years, a number of studies have shown that there is sexual dimorphism in the neuroendocrine and metabolic responses to physiological stress (11, 20). Compared with men, women appear to have a decreased sympathetic nervous system response to stress. The two manifestations where the sexual dimorphism has been the most pronounced involve the response of the sympathetic nervous system to fluid shifts and altered fuel metabolism during exercise, both of which are altered with spaceflight.
Entry into earth orbit causes a shift of water from the lower body to the upper body; the reverse occurs on reentry. On the ground, models of the fluid shifts have revealed gender-based differences in baseline cardiovascular function (14, 16), in the response to exercise (3, 21) and to bed rest (45) and the responses to orthostatic stress such as what occurs after going from the supine to erect positions (18, 47).
Apart from the well known fact that women tend to have more body fat than men, there are differences in how men and women mobilize fat (22, 35). The counterregulatory response to fasting and insulin-induced hypoglycemia is smaller in women than in men (1, 12, 13). Fuel metabolism during exercise is also different. When energy needs are high, as during exercise, women oxidize more lipid and less carbohydrate than men (8, 20, 30, 34). Furthermore, exercise is associated with significantly greater increases in epinephrine and norepinephrine secretion in men than women (12, 20).
Thus there is a considerable body of evidence to suggest that there is a sexual dimorphism in the response to a perturbation of homeostasis, be it in fluid/cardiovascular or energy metabolism. The objectives of this study were to investigate whether a similar sexual dimorphism is found in the response to spaceflight. To do so, we compared catecholamine excretion by male and female astronauts from two shuttle missions, the two similar Spacelab Life Sciences (SLS) missions, 1 (SLS1, 1991) and 2 (SLS2, 1993), for evidence of sexual dimorphism. To further evaluate the variability of the catecholamine response in men, we compared catecholamine excretion from the two SLS missions against the 1996 Life and Microgravity Sciences Mission (LMS) and the first 12 days of the 1973 Skylab missions. Skylab was a prototype space station that consisted of three similar missions of 28, 56, and 84 days (28).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Urine Sample Collections
Twenty-four-hour urines were collected before, during, and after spaceflight on the payload crew members of space shuttle missions SLS1, SLS2, and LMS. Dietary intake before, during, and after spaceflight was measured (for details, see Refs. 42-44). The urine volumes collected from these missions were divided among several investigators. On SLS1 and SLS2, there were a number of common assays to one or more investigator teams. The common assays were done by NASA, and NASA provided the results to the other groups as part of a data-sharing agreement. Among the common group of analyses were the urinary catecholamines. For the purposes of this study, the data set from SLS1/2 was incomplete, because it included data only from subjects who participated in an experiment to study fluid regulation (26). One subject flew on both missions, and only the samples from SLS1 were analyzed by NASA. For this study, we analyzed the samples from the second mission, SLS2, and LMS. We did all of the catecholamine analyses on the urine samples from the LMS crew by HPLC and electrochemical detection. Creatinine analyses were available from our previous studies.Statistical Analysis
Data in the text, tables, and figures are means ± SE, with the number of subjects in parentheses. Flight day 1 was not included in any of the analyses because of incomplete sample collection for some subjects and motion sickness. Statistical analyses were done by t-tests or one-way analysis of variance, as appropriate. Significance was accepted at P < 0.05. ![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
SLS1 and SLS2 were very similar shuttle missions. Data from shuttle flights SLS1 and SLS2 are often combined to give a larger sample size (9, 26, 40, 41). SLS1 was a 9-day mission, and SLS-2 was a reflight of SLS1 but with measurements made up to day 12 of the 16-day mission. The 17-day LMS shuttle flight was flown in 1996. One subject flew twice. The responses for this subject were similar on the two missions. On SLS1, the subject's inflight norepinephrine excretion was 96% of preflight; on SLS2 it was 91%. Because of the close agreement between the two missions, there is no effect on the statistical significance of the data with the use of either the mean or the individual values from SLS1/2. We used the data set from the second mission for this subject because more data (12 vs. 9 days) were available.
Tables 1 and
2 summarize the anthropometric and
dietary data for the SLS1/2 and LMS shuttle missions (42,
43). The values for nitrogen balance are estimates, because they
are based on urinary nitrogen and do not include fecal nitrogen losses.
All of the astronauts lost weight, although the LMS astronauts lost much more weight than the SLS1/2 crew members (Table 1). Nitrogen balance decreased inflight on all missions, with the decrease being
greatest for the LMS mission (Table 2).
|
|
Table 3 summarizes the effect of
spaceflight on norepinephrine and epinephrine excretion for the two
missions. No spaceflight-related changes were found with epinephrine.
Overall norepinephrine excretion was decreased inflight on both SLS1/2
and LMS. Separating out the SLS1/2 data by gender shows that
norepinephrine excretion was essentially unchanged with spaceflight in
women and substantially decreased with the men (Table 3 and Fig.
1). The difference between the men and
women on SLS1/2 was statistically significant (P < 0.05). The rate of norepinephrine excretion was relatively constant with time in earth orbit (Figs. 1 and 2).
After flight, there was a 1- to 2-day increase in norepinephrine but no
evidence of any gender effects (Table 3); neither was there any
difference in norepinephrine excretion on subsequent days postflight.
|
|
|
Figure 2 shows the time course of the norepinephrine changes during
spaceflight for the men on SLS1/2, LMS, and the three Skylab missions.
It is apparent from the figure that there was considerable variation in
norepinephrine excretion between missions for the men. The variation
appears to be mission rather than subject dependent. There were also
differences in energy intake and nitrogen balance between the two
missions (Table 4).
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The Database
The data set consists of three independent sets of measurements.The SLS1/2 mission. With the exception of the second sample set from the subject who flew twice, the SLS1/2 values were analyzed within a few weeks of collection. The other set from this subject was analyzed by us some 6 yr later.
The LMS mission.
The urines from the LMS mission and the exception mentioned above had
been stored for 4-6 yr at 70°C before being analyzed. As a
consequence, they had lost some of their activity. Because all samples
were treated the same, the data are still usable for comparative
purposes. For the one subject who was studied twice, the absolute
values were different with the NASA-provided SLS1/2 values (SLS1,
analyzed in 1991, preflight 4.6 ± 0.4 nM · kg
1 · day
1, 226 ± 24 nM · g creatinine · day
1) being
greater than the later (SLS2, analyzed in 2000, preflight 1.5 ± 0.1 nM · kg
1 · day
1,
77 ± 5 nM · g creatinine · day
1).
Nevertheless, the change with spaceflight was the same (96 vs. 91% of
the preflight value for the two missions).
Variability of the Norepinephrine Response
The two major findings from this investigation are the sexual dimorphism and that the norepinephrine excretion by men during spaceflight appears to be mission dependent. We shall discuss the variability in norepinephrine excretion by men first.The first report of norepinephrine excretion inflight was from the 1973 Skylab missions (28). Overall, a trend toward a decrease
in norepinephrine excretion was observed, but when broken out by
mission, the decrease was limited to the Skylab 4 crew (Fig.
3). A subsequent report on seven of the
SLS1/2 crew members by Leach et al. (26) concluded that
the overall excretion of norepinephrine was reduced inflight.
Norepinephrine excretion was reduced on the LMS crew members (Table 3
and Fig. 2, P < 0.05). Three effects acting in synergy
can explain the variability in norepinephrine excretion by men
inflight.
|
Decreased sympathetic response to the fluid shifts. The first effect is the decreased sympathetic response to the fluid shifts. Decreases in urinary norepinephrine secretion have been consistently documented in bed rest studies (4, 7, 10, 17, 26, 27). The reduction in norepinephrine secretion and the unchanged epinephrine have been attributed to the inhibition of sympathoneural outputs secondary to the increased cardiac filling from the head-directed fluid shifts (17, 39). However, this does not explain the difference between the LMS and SLS1/2 men (Fig. 2). Finding a difference between two spaceflight missions is not an artifact. Our reexamination of the earlier Skylab data revealed similar differences among the three Skylab missions (Fig. 2). As with SLS1/2 and LMS, norepinephrine excretion on Skylab varied with mission rather than subject. We have previously reported that dietary intake varied in a similar manner with mission (Fig. 3), with the cause of the difference being the amount of exercise required of the crew (41).
It is clear from Figs. 2 and 3 that the variation for both norepinephrine excretion and energy intake is between missions rather than subjects. The relevant point to the present discussion is that the differential norepinephrine response cannot be attributed to the fluid shifts or other cardiovascular-related changes. The fluid shifts and cardiovascular responses are unique to microgravity, and the microgravity environment was the same for all missions. The parallels between Figs. 2 (norepinephrine) and 3 (dietary intake) suggest that the variability of the norepinephrine response is related to fuel metabolism. The two aspects of fuel metabolism that can influence norepinephrine metabolism are energy balance and the ratio of glucose to fat in the diet.Energy balance. In previous analyses of differences in protein losses between the SLS1/2 and LMS missions, we showed that the missions were, in fact, very different in terms of dietary intake, workload, and energy balance (41). Briefly, SLS1/2 was a mission with moderate intake and no mandatory exercise requirement, with the subjects being in approximate energy balance. For Skylab, the exercise requirements were considerable, but dietary input was high, so subjects were only in mildly negative energy balance (36). On LMS, the workload from the required exercise program was high, dietary intake was low, and the astronauts were in serious negative energy balance.
For the SLS1/2 astronauts, endogenous lipid mobilization was minimal because they were in approximate energy balance (41). In contrast, the LMS astronauts were in negative energy balance (~15 kcal · kgRatio of carbohydrate to fat in the metabolic fuel mix. The Skylab norepinephrine data are different from those of either LMS or SLS1/2 (Fig. 2) but are consistent with our interpretation of the shuttle data. The three Skylab missions lasted 28, 56, and 84 days. Dietary intake and the amount of exercise done were increased from the 28-day mission to the 84-day mission. There was an apparent trend for the nitrogen losses to decrease with increasing energy intake (29, 37, 38).
On two of the three Skylab missions (missions 3 and 4), norepinephrine excretion was either unchanged or even increased with spaceflight (Fig. 2). Dietary intake was highest for the Skylab 4 astronauts, and they lost the least amount of protein and fat (29, 36). The implication is that they had less need to mobilize body fat; hence the lower norepinephrine excretion on Skylab 4. The energy intake deficits on Skylab missions 2 and 3 were far less than on LMS (Fig. 3), and the decrease in norepinephrine excretion was less (Fig. 2). The expected result is that the greater the energy deficit, the more norepinephrine activity to mobilize endogenous fat. Skylab 4 and SLS1/2 should be comparable, because in both cases, astronauts were in approximate energy balance, but norepinephrine excretion was greater on Skylab 4 (P < 0.05). The following explanation is suggested for these differences. Shuttle diets are significantly higher in carbohydrates than the astronauts' habitual diets or the diets provided to astronauts preflight (25). Table 4 gives the ratios of carbohydrate to fat in the diets of the SLS1/2 and LMS crews. Although the ratio of carbohydrate to fat intake was ~30%, greater inflight than preflight on SLS1/2, the increase was not statistically significant. The reason was that there was an outlier, who greatly increased fat intake inflight. For the other six subjects, the ratio preflight was 1.64 ± 0.09 and inflight was 2.39 ± 0.25 (P < 0.05). [For this subject the ratio of carbohydrate to fat decreased from 2.56 preflight to 1.67 inflight. In a previous report, we had identified this particular individual as having an anomalous pattern of dietary intake inflight. This individual's dietary intake remained depressed on flight day 2 (Fig. 4 in Ref. 43) and then increased steadily until the end of the mission when intake was ~50% greater than the mean preflight intake]. In the fed state, the fuel mix oxidized by the cells reflects the diet but is not wholly derived from the diet. The source of fatty acids oxidized by the tissues is a mixture of dietary and adipose tissue triglycerides because of the continuous free fatty acid-triacylglycerol cycling that occurs. As a result of fatty acid-triacylglycerol cycling, only a proportion of dietary lipids is oxidized in the period immediately after ingestion (6). Even at rest, fatty acid release exceeds oxidation about twofold (19, 23). The amount of fat oxidized depends on the regulation of lipolysis, which is subject to regulation by norepinephrine. Thus increasing the proportion of carbohydrate in the diet at the expense of fat will depress free fatty acid-triacylglycerol cycling via a decrease in norepinephrine activity. There was no carbohydrate-to-fat effect on Skylab, because the subjects were on a controlled diet before and during flight; hence the lower norepinephrine excretion on the two shuttle flights. For the shuttle missions, diet was monitored but not controlled, and for unknown reasons, all but one of the shuttle crew members selected diets low in fat.Sexual dimorphism.
Our analysis of the SLS1/2 norepinephrine data showed a statistically
significant difference in the responses of men and women (Table 2 and
Fig. 1). There were no differences in energy intake or N balance. There
was a large reduction in norepinephrine excretion inflight for the men
(41 ± 9% of preflight) and no change with the women (98 ± 10%, P < 0.05). Although the number of women was small (n = 3), the data showing a difference in
response between men and women is statistically significant, and there
was adequate power (Table 3, F = 8.45, = 0.05, power = 0.82). The result with women was reproducible. As we have
pointed out, the results were similar for the subject who flew on both
SLS1 and SLS2.
![]() |
ACKNOWLEDGEMENTS |
---|
We thank Dr. Warren Biele, M. J. Leskiw, and M. D. Schluter for technical assistance and the staff of the Nutrition and Metabolism laboratory at the Johnson Space Center for providing us with the SLS1/2 data.
![]() |
FOOTNOTES |
---|
This study was supported by NASA contracts NAS 9-18775 and NAG 9-1162.
Address for reprint requests and other correspondence: T. P. Stein, Dept. of Surgery, Univ. of Medicine and Dentistry of New Jersey, School of Osteopathic Medicine, 2 Medical Center Dr., Stratford, NJ 08084 (E-mail: tpstein{at}umdnj.edu).
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.
Received 23 February 2001; accepted in final form 20 April 2001.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Amiel, SA,
Maran A,
Powrie JK,
Umpleby AM,
and
Macdonald IA.
Gender differences in counterregulation to hypoglycaemia.
Diabetologia
36:
460-464,
1993[ISI][Medline].
2.
Arias-Stella, J.
Chronic mountain sickness: pathology and definition.
In: High Altitude Physiology: Cardiac and Respiratory Aspects, edited by Porter RJ,
and Knight J. Edinburgh, UK: Churchill Livingston, 1971, p. 31-40.
3.
Astrand, P,
Cuddy T,
Saltin B,
and
Stenberg J.
Cardiac output during submaximal and maximal work.
J Appl Physiol
19:
268-273,
1964[ISI].
4.
Barbe, P,
Galitzky J,
Thalamas C,
Langin D,
Lafontan M,
Senard JM,
and
Berlan M.
Increase in epinephrine-induced responsiveness during microgravity simulated by head-down bed rest in humans.
J Appl Physiol
87:
1614-1620,
1999
5.
Barnett, SR,
Morin RJ,
Kiely DK,
Gagnon M,
Azhar G,
Knight EL,
Nelson JC,
and
Lipsitz LA.
Effects of age and gender on autonomic control of blood pressure dynamics.
Hypertension
33:
1195-1200,
1999
6.
Binnert, C,
Pachiaudi C,
Beylot M,
Croset M,
Cohen R,
Riou JP,
and
Laville M.
Metabolic fate of an oral long-chain triglyceride load in humans.
Am J Physiol Endocrinol Metab
270:
E445-E450,
1996
7.
Blanc, S,
Normand S,
Ritz P,
Pachiaudi C,
Vico L,
Gharib C,
and
Gauquelin-Koch G.
Energy and water metabolism, body composition, and hormonal changes induced by 42 days of enforced inactivity and simulated weightlessness.
J Clin Endocrinol Metab
83:
4289-4297,
1998
8.
Blatchford, FK,
Knowlton RG,
and
Schneider DA.
Plasma FFA responses to prolonged walking in untrained men and women.
Eur J Appl Physiol
53:
343-347,
1985.
9.
Buckey, JC, Jr,
Lane LD,
Levine BD,
Watenpaugh DE,
Wright SJ,
Moore WE,
Gaffney FA,
and
Blomqvist CG.
Orthostatic intolerance after spaceflight.
J Appl Physiol
81:
7-18,
1996
10.
Convertino, VA.
Physiological adaptations to weightlessness: effects on exercise and work performance.
Exerc Sport Sci Rev
18:
119-166,
1990[Medline].
11.
Davis, SN,
Galassetti P,
Wasserman DH,
and
Tate D.
Effects of gender on neuroendocrine and metabolic counterregulatory responses to exercise in normal man.
J Clin Endocrinol Metab
85:
224-230,
2000
12.
Davis, SN,
Goldstein RE,
Price L,
Jacobs J,
and
Cherrington AD.
The effects of insulin on the counterregulatory response to equivalent hypoglycemia in patients with insulin-dependent diabetes mellitus.
J Clin Endocrinol Metab
77:
1300-1307,
1993[Abstract].
13.
Diamond, MP,
Jones T,
Caprio S,
Hallarman L,
Diamond MC,
Addabbo M,
Tamborlane WV,
and
Sherwin RS.
Gender influences counterregulatory hormone responses to hypoglycemia.
Metabolism
42:
1568-1572,
1993[ISI][Medline].
14.
Freedman, RR,
Sabharwal SC,
and
Desai N.
Sex differences in peripheral vascular adrenergic receptors.
Circ Res
61:
581-585,
1987[Abstract].
15.
Galster, AD,
Clutter WE,
Cryer PE,
Collins JA,
and
Bier DM.
Epinephrine plasma thresholds for lipolytic effects in man: measurements of fatty acid transport with [1-13C]palmitic acid.
J Clin Invest
67:
1729-1738,
1981[ISI][Medline].
16.
Gillum, RF.
The epidemiology of resting heart rate in a national sample of men and women: associations with hypertension, coronary heart disease, blood pressure, and other cardiovascular risk factors.
Am Heart J
116:
163-174,
1988[ISI][Medline].
17.
Goldstein, DS,
Vernikos J,
Holmes C,
and
Convertino VA.
Catecholaminergic effects of prolonged head-down bed rest.
J Appl Physiol
78:
1023-1029,
1995
18.
Gotshall, RW,
Tsai PF,
and
Frey MA.
Gender-based differences in the cardiovascular response to standing.
Aviat Space Environ Med
62:
855-859,
1991[ISI][Medline].
19.
Horowitz, JF,
and
Klein S.
Lipid metabolism during endurance exercise.
Am J Clin Nutr
72:
558S-563S,
2000
20.
Horton, TJ,
Pagliassotti MJ,
Hobbs K,
and
Hill JO.
Fuel metabolism in men and women during and after long-duration exercise.
J Appl Physiol
85:
1823-1832,
1998
21.
Hossack, KF,
and
Bruce RA.
Maximal cardiac function in sedentary normal men and women: comparison of age-related changes.
J Appl Physiol
53:
799-804,
1982
22.
Jones, PP,
Snitker S,
Skinner JS,
and
Ravussin E.
Gender differences in muscle sympathetic nerve activity: effect of body fat distribution.
Am J Physiol Endocrinol Metab
270:
E363-E366,
1996
23.
Klein, S,
Young VR,
Blackburn GL,
Bistrian BR,
and
Wolfe RR.
Palmitate and glycerol kinetics during brief starvation in normal weight young adult and elderly subjects.
J Clin Invest
78:
928-933,
1986[ISI][Medline].
24.
Kurpad, AV,
Khan K,
Calder AG,
and
Elia M.
Muscle and whole body metabolism after norepinephrine.
Am J Physiol Endocrinol Metab
266:
E877-E884,
1994
25.
Lane, HW.
Energy requirements for spaceflight.
J Nutr
122:
13-18,
1992[ISI][Medline].
26.
Leach, CS,
Alfrey CP,
Suki WN,
Leonard JI,
Rambaut PC,
Inners LD,
Smith SM,
Lane HW,
and
Krauhs JM.
Regulation of body fluid compartments during short-term spaceflight.
J Appl Physiol
81:
105-116,
1996
27.
Leach, CS,
Altchuler SI,
and
Cintron-Trevino NM.
The endocrine and metabolic responses to space flight.
Med Sci Sports Exerc
15:
432-440,
1983[ISI][Medline].
28.
Leach, CS,
and
Rambaut PC.
Biomedical responses of the Skylab crewmen: an overview.
In: Biomedical Results from Skylab (NASA SP-377), edited by Johnson RS,
and Dietlein LF. Washington, DC: GPO, 1977, p. 204-217.
29.
Leonard, JI,
Leach CS,
and
Rambaut PC.
Quantitation of tissue loss during prolonged spaceflight.
Am J Clin Nutr
38:
667-679,
1983[Abstract].
30.
MacDougall, JD,
Tarnopolsky MA,
Chesley A,
and
Atkinson SA.
Changes in muscle protein synthesis following heavy resistance exercise in humans: a pilot study.
Acta Physiol Scand
146:
403-404,
1992[ISI][Medline].
31.
Milley, JR.
Ovine fetal metabolism during norepinephrine infusion.
Am J Physiol Endocrinol Metab
273:
E336-E347,
1997
32.
Pequignot, JM,
Guell A,
Gauquelin G,
Jarsaillon E,
Annat G,
Bes A,
Peyrin L,
and
Gharib C.
Epinephrine, norepinephrine, and dopamine during a 4-day head-down bed rest.
J Appl Physiol
58:
157-163,
1985
33.
Pequignot, JM,
Spielvogel H,
Caceres E,
Rodriguez A,
Sempore B,
Pequignot J,
and
Favier R.
Influence of gender and endogenous sex steroids on catecholaminergic structures involved in physiological adaptation to hypoxia.
Pflügers Arch
433:
580-6,
1997[ISI][Medline].
34.
Phillips, SM,
Atkinson SA,
Tarnopolsky MA,
and
MacDougall JD.
Gender differences in leucine kinetics and nitrogen balance in endurance athletes.
J Appl Physiol
75:
2134-2141,
1993[Abstract].
35.
Poehlman, ET,
Gardner AW,
Goran MI,
Arciero PJ,
Toth MJ,
Ades PA,
and
Calles-Escandon J.
Sympathetic nervous system activity, body fatness, and body fat distribution in younger and older males.
J Appl Physiol
78:
802-806,
1995
36.
Rambaut, PC,
Leach CS,
and
Leonard JI.
Observations in energy balance in man during spaceflight.
Am J Physiol Regulatory Integrative Comp Physiol
233:
R208-R212,
1977[ISI][Medline].
37.
Rambaut, PC,
Leach CS,
and
Whedon GD.
A study of metabolic balance in crew members of Skylab IV.
Acta Astronaut
6:
1313-1322,
1979[ISI][Medline].
38.
Rambaut, PC,
Smith MC, Jr,
Leach CS,
Whedon GD,
and
Reid J.
Nutrition and responses to zero gravity.
Fed Proc
36:
1678-1682,
1977[ISI][Medline].
39.
Robertson, D,
Hollister AS,
Carey EL,
Tung CS,
Goldberg MR,
and
Robertson RM.
Increased vascular beta2-adrenoceptor responsiveness in autonomic dysfunction.
J Am Coll Cardiol
3:
850-856,
1984[ISI][Medline].
40.
Shykoff, BE,
Farhi LE,
Olszowka AJ,
Pendergast DR,
Rokitka MA,
Eisenhardt CG,
and
Morin RA.
Cardiovascular response to submaximal exercise in sustained microgravity.
J Appl Physiol
81:
26-32,
1996
41.
Stein, TP.
The relationship betwen dietary intake, exercise, energy balance and thermoregulation during spaceflight.
Pflügers Arch Eur J Physiol
551:
R21-R31,
2000.
42.
Stein, TP,
Leskiw MJ,
and
Schluter MD.
Diet and nitrogen metabolism during spaceflight on the shuttle.
J Appl Physiol
81:
82-97,
1996
43.
Stein, TP,
Leskiw MJ,
Schluter MD,
Hoyt RW,
Lane HW,
Gretebeck RE,
and
LeBlanc AD.
Energy expenditure and balance during spaceflight on the shuttle: the LMS mission.
Am J Physiol Regulatory Integrative Comp Physiol
276:
R1739-R1748,
1999
44.
Stein, TP,
Schluter MD,
and
Moldawer LL.
Endocrine relationships during human spaceflight.
Am J Physiol Endocrinol Metab
276:
E155-E162,
1999
45.
Vernikos, J,
Dallman MF,
Keil LC,
O'Hara D,
and
Convertino VA.
Gender differences in endocrine responses to posture and 7 days of 6 degrees head-down bed rest.
Am J Physiol Endocrinol Metab
265:
E153-E161,
1993
46.
Whedon, G,
Lutwak L,
Rambaut P,
Whittle M,
Smith MC,
Read J,
Leach CS,
Stadler CR,
and
Sanford DD.
Mineral and nitrogen metabolic studies, Experiment M071.
In: Biomedical Results from Skylab (NASA SP-377), edited by Johnson RS,
and Dietlein LF. Washington, DC: GPO, 1977, sect. 3, p. 164-174.
47.
White, M,
Courtemanche M,
Stewart DJ,
Talajic M,
Mikes E,
Cernacek P,
Vantrimpont P,
Leclerc D,
Bussières L,
and
Rouleau JL.
Age- and gender-related changes in endothelin and catecholamine release, and in autonomic balance in response to head-up tilt.
Clin Sci (Colch)
93:
309-316,
1997[ISI][Medline].