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1 Metabolism, ABSTRACT Ferrando, Arny A., Kevin D. Tipton, Marcas M. Bamman, and
Robert R. Wolfe. Resistance exercise maintains skeletal muscle protein synthesis during bed rest. J. Appl.
Physiol. 82(3): 807-810, 1997.
spaceflight; microgravity; biopsy
INTRODUCTION PROLONGED INACTIVITY or bed rest has been shown to
result in loss of body nitrogen (10, 12, 23, 25) and lean body mass (9,
13, 23, 26). This loss of lean body mass is most prevalent in the
ambulatory muscle groups (13, 19). Because the bed rest-induced loss
mimics that resulting from spaceflight (20), it is often used as a
ground-based model to study the effects of microgravity (16). Although
the basis for a loss of lean body mass in microgravity remains unclear,
bed rest has been shown to decrease skeletal muscle protein synthesis
(MPS) (12). Thus interventions known to increase MPS, such as
resistance exercise (6, 7, 21), might be of potential benefit. Previous studies (7, 21) noted a doubling of MPS after an acute bout of
resistance exercise. Thus it was hypothesized that resistance training
throughout bed rest could ameliorate the effects of bed rest on MPS.
MATERIALS AND METHODS
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
Spaceflight
results in a loss of lean body mass and muscular strength. A
ground-based model for microgravity, bed rest, results in a loss of
lean body mass due to a decrease in muscle protein synthesis (MPS).
Resistance training is suggested as a proposed countermeasure for
spaceflight-induced atrophy because it is known to increase both MPS
and skeletal muscle strength. We therefore hypothesized that scheduled
resistance training throughout bed rest would ameliorate the decrease
in MPS. Two groups of healthy volunteers were studied during 14 days of
simulated microgravity. One group adhered to strict bed rest (BR;
n = 5), whereas a second group engaged
in leg resistance exercise every other day throughout bed rest (BREx;
n = 6). MPS was determined directly by
the incorporation of infused
L-[ring-13C6]phenylalanine
into vastus lateralis protein. After 14 days of bed rest, MPS in the
BREx group did not change and was significantly greater than in the BR
group. Thus moderate-resistance exercise can counteract the decrease in
MPS during bed rest.
1) measure of MPS. This was followed by 14 days of strict 6° head-down bed rest. A second determination of MPS
was made on bed rest day 14 (BR 14).
The head-down tilt was utilized to simulate the effects of microgravity on initial fluid volume shifts (15) for unrelated studies. Subjects were not permitted to deviate from this position and were monitored continuously by the GCRC staff.
1.1 g protein · kg body
wt
1 · day1.
Resistance training.
The knee extensors were exercised isotonically every other day during
bed rest from the supine position by utilizing a horizontal leg-training device (Cybex Strength Systems, Ronkonkoma, NY). Resistance exercise subjects were first familiarized with the training
protocol 1 day before bed rest. After learning the proper exercise
form, subjects practiced by completing 3 sets of 10-12 repetitions. To preclude the likelihood of studying the effects of
acute resistance exercise on MPS (7), the final training session (BR
13) again consisted of 3 sets of 10-12 repetitions.
During bed rest, muscle soreness was minimized in these untrained
subjects by progressively increasing volume and intensity during the
first three sessions. By session 3,
five sets to volitional muscle failure were completed. The number of
repetitions for all sets was set at 8 (range 7-9) throughout
training. If a set was performed outside this range, the load of
subsequent sets was adjusted accordingly. Progressive resistance was
therefore incorporated into the program. Exercise was performed at a
volume and intensity known to effectively induce gains in strength and
muscle mass (1, 18). Rest between sets was set at 90 s to permit
restoration of creatine phosphate (27). Loads for warm-ups were set at
two-thirds of the previous training session's eight repetition maximum
(RM). All training was supervised by one of the investigators.
Pre- and post-bed rest strength were measured (BREx group only) by 1 RM
on the same training device. Pre- and post-bed rest strength were also
measured in a separate control group of a similarly designed but
unrelated study by one of the investigators (3). Identical equipment
and strength-testing procedures were utilized, and the comparison of
strength variables with the current BREx group are presented in
DISCUSSION. After sufficient warm-up,
sets of 1 RM were executed with increasing resistance until a subject failed on two consecutive attempts at a given load. The greatest load
lifted successfully was then recorded as 1 RM. Trials were separated by
2-3 min. The range of motion of each movement was standardized for
each subject and repeated post-bed rest. Each determination of 1 RM was
performed after the infusion protocol described below.
Skeletal MPS.
We examined the effects of bed rest and bed rest plus resistance
exercise on MPS. On days BR 1 and BR 14 after a 12-h fast, a
catheter was inserted into an antecubital vein for stable isotope infusion. Subjects received a 5-h primed (2 µmol/kg) continuous (0.05 µmol · kg1 · min1)
infusion of
L-[ring-13C6]phenylalanine
(Phe; 99% enriched; Cambridge Isotope Laboratories, Woburn, MA).
Subjects were recumbent and horizontal throughout the 5-h infusion
period. At 2 h, a muscle needle biopsy was taken from the lateral
portion of the vastus lateralis to measure isotopic carbon enrichment
of bound and free Phe in the muscle. A second biopsy was performed at
the end of the study at 5 h. Biopsies were performed according to the
Bergström technique as previously described (5).
MPS was calculated from the determination of the rate of tracer
incorporation into the protein and the enrichment of the intracellular pool as the precursor
![MPS = [(E<SUB>p 2</SUB> − E<SUB>p 1</SUB>) × 1.5/(E<SUB>M</SUB> × <IT>t</IT>)] × 60 × 100](/content/vol82/issue3/fulltext/807/img001.gif)
|
70°C
until processed. The tissue was weighed and protein was precipitated
with 0.5 ml of 10% perchloric acid. The tissue was then homogenized
and centrifuged, and the supernatant was collected. This procedure was
repeated two more times, and the pooled supernatant (1.3 ml) was
stored at 70°C until analysis.
The remaining pellet of muscle tissue was further washed three times
with absolute ethanol and twice in 0.9% saline. It was then placed
overnight in an oven and dried at 50°C. The dried pellet was then
hydrolyzed at 110°C for 36 h with 6 N HCl. The protein hydrolysate
was then passed through acid-washed Celite to remove carbon particles.
Phe was isolated and purified from the filtered solution by
high-pressure liquid chromatography (LKB Bromma). Samples containing
pure Phe were dried under nitrogen, placed in tin containers, and
combusted by using a carbon-nitrogen analyzer (Nitrogen Analyzer 1500, Carlo Erba, Serono, Italy). After combustion, the
CO2 was automatically injected
into an isotope ratio mass spectrometer (VG Isogas, Middlewich, UK) for
determination of the
13C/12C
ratio in protein-bound Phe. The precision of this procedure has been
previously reported (5).
On thawing, the pooled supernatant of cellular water was passed over a
cation-exchange column (Dowex AG 50W-8X, 100- to 200- mesh
H+ form; Bio-Rad, Richmond, CA)
and dried under vacuum by using a Speed Vac (Savant Instruments,
Farmingdale, NY). One hundred microliters of
N-methyl-N-(tert-butyldimethylsilyl)
trifluoroacetamide (Pierce, Rockford, IL) and 100 µl of acetonitrile
were added to the dry residue. The mixture was then heated at 95°C
for 45 min. The isotopic enrichment of the in vivo labeled Phe was
determined by using an HP 5890/5989B GC/MS engine (Hewlett-Packard,
Palo Alto, CA). The ions 234 and 240 (mass-to-charge ratio) were
selectively monitored to determine precursor Phe enrichment.
Data presentation and statistical analysis.
Data are presented as means ± SE. BR 1 and BR 14 MPS and
1-RM values in each group were compared by paired
t-test. The change in MPS from BR 1 to BR 14 for each group was compared between groups by
t-test. A
P value 
0.05 was considered
statistically significant.
RESULTS
Bed rest resulted in a 46% decrease in MPS in the BR group (0.074 ± 0.011 to 0.040 ± 0.007%/h;
P < 0.04). However, resistance exercise maintained MPS in the BREx group (0.066 ± 0.011 to 0.094 ± 0.026%/h; P = 0.20) (Fig.
1). The demonstrated change in MPS from the
beginning to the end of bed rest was significantly different between
groups (P < 0.04). The BR group
experienced a mean decrease of 0.034 ± 0.015%/h, whereas MPS in
the BREx group demonstrated a nonsignificant increase of 0.028 ± 0.019%/h.
1) and after
14 days of bed rest (BR 14) in control subjects (solid bars) and
subjects engaging in resistance training (crosshatched bars). * Significantly different vs. BR 1, P < 0.04.
1-RM strength was maintained in the BREx group (208.3 ± 14.7 kg pre-bed rest vs. 214.2 ± 12.3 kg post-bed rest, respectively; P = 0.65).
DISCUSSION
Acute bouts of resistance training have been shown to double protein synthesis up to 24 h postexercise (7, 21). Because the subjects in this study engaged in resistance training every other day, the intent was to maintain a stimulation of MPS such that the noted decrease with inactivity could be prevented (12). The present study demonstrates the cumulative effects of repeated stimulation of MPS. In addition to the elimination of a decreased MPS, this exercise protocol maintained muscle strength.
Muscular unloading by inactivity or bed rest has been shown to decrease muscle strength (26). In particular, locomotor muscle strength is compromised with the continued unloading of bed rest (3, 26). In this respect, bed rest is a viable ground-based model for the perturbations of spaceflight (20). Weightlessness results in a more-pronounced loss of strength in the legs, particularly in the knee extensors (8). The ability to maintain strength and function in the locomotor muscle groups is of prime concern to the astronaut. Impaired muscle function is detrimental to the astronaut's ability to perform shuttle landing, egress, and extravehicular activity with prolonged exposure to microgravity. Thus a countermeasure that is effective in ameliorating these losses would enhance the astronaut's performance capability.
On the basis of the results of the present study and resistance training's established influence on muscle strengthening (1) and MPS (6, 7, 21), it is tempting to speculate that a relationship exists between the chronic stimulation of skeletal MPS and muscular strength. This notion is supported by the results of previous studies analyzing the effects of inactivity or immobilization on MPS and strength. An identical research protocol as the present study (with bed rest only) demonstrated a decrease in 1-RM leg extensor strength (229.1 ± 7.4 kg pre-bed rest vs. 208.0 ± 8.2 kg post-bed rest, respectively; P < 0.01) (3). The present study provides evidence that the decrease in strength corresponds to a decreased fractional synthetic rate of protein synthesis. With muscular stimulation, however, the relationship between MPS and strength is maintained. In addition to the present findings, Gibson et. al (14) noted that the fractional synthetic rate of muscle protein and fiber cross-sectional area could be maintained in the casted (immobilized) leg by electrical stimulation. Electrical stimulation has also been shown to prevent reductions in leg volume, muscle compartment size, and muscle strength with bed rest (11).
These findings, however, do not establish a direct relationship between MPS and strength. Indeed, MPS is greatly increased immediately after resistance exercise (6), yet it cannot be suggested that strength would acutely increase. Rather, the relationship between MPS and muscular strength is most likely dependent on a net MPS balance over time. Circumstances resulting in hypermetabolism, such as burn injury, will produce elevated protein synthetic rates yet a net loss in skeletal muscle protein and strength (22). Resistance exercise alone provides a more favorable net muscle protein balance (6), which could be further enhanced by hyperinsulinemia and hyperaminoacidemia (4). The limited data involving spaceflight have shown an increase in whole body protein synthesis (24), yet spaceflight is known to result in a loss of lean body mass (20) and strength (8). Protein breakdown was not assessed in this study; however, previous work has demonstrated that the loss of lean body mass (12) and strength (3) during bed rest is a result of altered protein balance (12). Thus periodic stimulation of MPS with resistance exercise most likely results in a positive net protein balance over time that preserves muscle strength.
Most importantly, this study illustrates that scheduled periodic resistance exercise will prevent the decline in MPS and strength with inactivity. The results of the present study indicate that resistance training may be a viable countermeasure to the loss of muscle strength and mass with spaceflight (2). Endurance exercise is currently employed in space; however, it is unsuccessful in ameliorating reductions in muscle strength (17). Resistive devices are currently being developed but have yet to be flown as a countermeasure. This study suggests that repeated stimulation of MPS, or most likely the maintenance of net protein synthesis, may be integral to the maintenance of muscular strength.
ACKNOWLEDGEMENTS
The authors thank the National Aeronautics and Space Administration for its support and emphasis on this area of research and the nursing staff at the University of Texas Medical Branch General Clinical Research Center for their tireless efforts and meticulous care of subjects.
FOOTNOTES
Address for reprint requests: A. A. Ferrando, Metabolism, Shriners Burns Institute, 815 Market St., Galveston, TX 77550.
Received 13 September 1996; accepted in final form 1 November 1996.
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M. S. F. Clarke, M. M. Bamman, and D. L. Feeback Bed rest decreases mechanically induced myofiber wounding and consequent wound-mediated FGF release J Appl Physiol, August 1, 1998; 85(2): 593 - 600. [Abstract] [Full Text] [PDF]
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M. M. Bamman, M. S. F. Clarke, D. L. Feeback, R. J. Talmadge, B. R. Stevens, S. A. Lieberman, and M. C. Greenisen Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution J Appl Physiol, January 1, 1998; 84(1): 157 - 163. [Abstract] [Full Text] [PDF]
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