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1 Department of Physiology and
Pharmacology, ABSTRACT Berg, H. E., L. Larsson, and P. A. Tesch. Lower limb
skeletal muscle function after 6 wk of bed rest. J. Appl. Physiol. 82(1): 182-188, 1997.
atrophy; electromyography; humans; inactivity; maximum voluntary
strength
INTRODUCTION THE GRAVITY-DEPENDENT LOAD of the human body, acting on
the lower limbs in the upright position, seems fundamental to
maintenance of lower limb skeletal muscle function. Thus reduced
weight-bearing activity per se, either on experimental
cast immobilization (cf. Ref. 10), lower limb unloading (2, 3, 6, 11),
bed rest (12, 18), or extended stay in weightlessness (33) results in
substantial muscle dysfunction within a few weeks.
Muscle atrophy, resulting from loss of contractile proteins, is one
well-recognized cause of such functional impairment but appears to
explain only about two-thirds of the strength loss shown after 1 mo of
bed rest (25) or unilateral lower limb unloading (3, 11). Among
candidates to explain the disproportionate strength loss are decreased
neural drive (cf. Ref. 27) and decreased force-generating capacity of
muscle (6).
In an attempt to distinguish the potential factors that might be
responsible for the observed muscle dysfunction and to quantify their
relative importance for adaptation in response to long-term muscle
unloading, volunteers subjected to 6 wk of bed rest were studied.
Maximal voluntary knee-extension torque and velocity and
electromyographic (EMG) activity during knee extension were assessed
before and after bed rest. Knee extensor cross-sectional area (CSA) was
assessed by using magnetic resonance imaging (MRI).
It has repeatedly been reported that unloaded animal muscle
undergoes alterations in contractile properties such that there is an
increase in maximum shortening velocity and a corresponding shift in
the force-velocity relationship of slow-twitch muscle (cf. Ref. 17).
These changes typically coincide with an increased fast-myosin content
or transformation from type I to type II fibers. Experimental support
for extending these principles to humans is, however, poor (cf. Ref.
2). In fact, there are as yet no data available that describe in detail
the effects of unloading on muscle function along with myosin and fiber
type composition in humans.
Although muscle fiber type transformation may occur in response to
hindlimb suspension in rats (cf. Ref. 30), potentially altering
skeletal muscle force-velocity characteristics, human studies employing
standard enzyme histochemistry have not disclosed such an adaptation
(2, 4, 20, 21). Therefore, skeletal muscle fiber type and myosin heavy
chain (MHC) isoforms were examined.
More specifically, the purpose of the study was to describe the
magnitude and characteristics of the strength decline in response to
bed rest while quantifying the concomitant changes in neural drive and
muscle mass and morphology.
It was hypothesized that 6 wk of bed rest would result in a marked
reduction in maximum voluntary isometric and dynamic force. We expected
to disclose a significant muscle atrophy that would nevertheless not
fully account for the strength loss and that, as a consequence, force
per knee extensor muscle CSA would be decreased. It was also
hypothesized that knee extensor fiber type and MHC composition of the
vastus lateralis muscle would not be affected by bed rest and therefore
that concomitant changes in force-velocity characteristics of the knee
extensor muscle group would most likely not occur.
METHODS
Force,
electromyographic (EMG) activity, muscle mass, and fiber
characteristics were studied in seven healthy men before and after 6 wk
of bed rest. Maximum voluntary isometric and concentric knee extensor
torque decreased (P < 0.05)
uniformly across angular velocities by 25-30% after bed rest.
Maximum quadricep rectified EMG decreased by 19 ± 23%, whereas
submaximum (100-Nm isometric action) EMG increased by 44 ± 28%.
Knee extensor muscle cross-sectional area (CSA), assessed by using
magnetic resonance imaging, decreased by 14 ± 4%. Maximum torque
per knee extensor CSA decreased by 13 ± 9%. Vastus lateralis fiber
CSA decreased 18 ± 14%. Neither type I, IIA, and IIB fiber
percentages nor their relative proportions of myosin heavy chain (MHC)
isoforms were altered after bed rest. Because the decline in strength
could not be entirely accounted for by decreased muscle CSA, it is
suggested that the strength loss is also due to factors resulting in
decreased neural input to muscle and/or reduced specific
tension of muscle, as evidenced by a decreased torque/EMG ratio.
Additionally, it is concluded that muscle unloading in humans does not
induce important changes in fiber type or MHC composition or in vivo
muscle contractile properties.
6°) bed rest.
)
were used for comparisons. EMG values were normalized to preunloading,
by using the mean of the three baseline measurements for each muscle
separately, and then averaged. Electromechanical efficiency was defined
as torque divided by
for a specific time average (see above).
Across the baseline sessions, there was no change in maximum
(P = 0.25) or submaximum
(P = 0.99) isometric torque. The CV across sessions and trials were 6.2 and 2.2% for isometric maximum and
0.8 and 0.6% for submaximum torque, respectively. The corresponding CV
for maximum 
were 10.9 and 8.1% and
for submaximum 12.8 and 6.1%,
respectively. For maximum torque/ ratio,
the CV were 9.6 and 9.8%, whereas submaximum
torque/
varied 13.4 and 7.1% between sessions and trials, respectively.
Muscle biopsy.
The percutaneous conchotome method was used to obtain tissue samples
from the left vastus lateralis muscle before and toward the end
(day 37) of bed rest.
Specimens, obtained after 60 min of supine rest, were frozen in freon
chilled with liquid nitrogen and stored at 80°C until
processed further (for details of biopsy preparations and techniques,
see Refs. 4, 23).
For enzyme-histochemical analysis, frozen muscle samples were cut at
their greatest girth perpendicular to the long axis of fiber
orientation in 10-µm serial sections by using a cryostat. Cross
sections were stained for myofibrillar adenosinetriphosphatase (ATPase)
and classified as type I, IIA, IIB, or IIC by using standard preincubations (pH 4.35, 4.5, 9.4). Fiber type classification of the
majority of fibers on each cross section (average fiber no. = 523;
range 205-1,371) was performed from magnified photographs of
myofibrillar ATPase-stained cross sections or directly from the
microscope via a TV overlay.
The CSA of individual muscle fibers was measured semiautomatically from
photographs. Each fiber was manually encircled, and CSA was calculated
by using computerized planimetry (Videoplan, Kontron, Munich, Germany).
Fiber CSA and diameter were estimated from 30 fibers of each type. Type
IIC fibers were ignored because they were seldom encountered. The mean
fiber area and diameter were calculated for each individual on the
basis of type I, IIA, and IIB fiber percentages and CSA. Analogously,
the relative CSA occupied by type I fibers was calculated.
MHC composition was determined in 10-µm serial sections by
one-dimensional sodium dodecyl sulfate-polyacrylamide gel
electrophoresis (SDS-PAGE; cf. Ref. 23; Fig.
1). To identify and determine the relative
content of different myofibrillar proteins, the separating gels were
silver stained and scanned in a soft-laser densitometer (4,096 optical
density levels, 50-µm pixel spacing; Molecular Dynamics, Sunnyvale,
CA) interfaced with a computer. With the use of the volume-integration
function (ImageQuant software version 3.3, Molecular Dynamics), type I,
IIA, and IIB MHC content was estimated and expressed in percentage of
total MHC in that sample.
MRI tomography. Muscle CSA was assessed before and toward the end (day 37) of bed rest by using MRI (Siemens Somatom Impact 1.5 T, Erlangen, Germany). Subjects were positioned with their thighs in the horizontal plane, and a foot restraint was used for fixation. Transaxial scans (10 mm, repetition time/echo time = 700/17 ms) were obtained equidistant from the most proximal and distal aspects of the femoral bone (midthigh), as estimated from frontal and sagittal scout images. The knee extensor muscle was manually encircled, and CSA was calculated by using computerized planimetry (National Institutes of Health Image 1.60, Macintosh Quadra 700). To prevent fluid shifts from influencing CSA secondary to a change in body position (5), subjects remained supine for 60 min before imaging preceding bed rest. Statistics. Repeated-measures analysis of variance was performed on functional parameters, including EMG, and on MRI data, and single-contrast means comparisons were used to evaluate effects of unloading. The paired t-test was used to evaluate differences in muscle biopsy parameters before and after bed rest. Correlation coefficients (r) were calculated from individual values after performance of linear-regression analyses. The variance of a selected parameter was calculated for each individual across the two consecutive trials or between means across the three test sessions, respectively. The square root of that group average, normalized by using the overall mean, expressed the CV. Statistical significance was set at P < 0.05. Values are reported as means ± SD.
RESULTS
decreased (P < 0.05; Fig. 2) by 19.4 ± 23.5%, whereas submaximum
increased (P < 0.05) by 44.4 ± 27.6% after bed rest. Submaximum
torque/
decreased (P < 0.05) by 23.2 ± 20.2% after bed rest. Maximum
torque/ did not change (P = 0.36).
Knee extensor angular velocity. Knee extensor AVmax decreased (5.1 ± 6.3%; P < 0.05) from 864 ± 79 to 816 ± 50°/s after bed rest. Muscle proteins, fiber types, and size. Mean fiber area and diameter decreased (P < 0.05) by 17.6 ± 13.6 and 7.8 ± 9.0%, respectively, after bed rest (Table 1). Type I CSA and diameter decreased (P < 0.05) by 18.2 ± 13.9 and 10.3 ± 7.9%, respectively. Type IIA (P = 0.26) and IIB (P = 0.08) fibers showed no change. Type I, IIA, and IIB muscle fiber percentages averaged 52.6 ± 10.3, 26.9 ± 9.9, and 20.2 ± 6.6%, respectively, before bed rest and were not altered (P = 0.66, 0.98, 0.21 for type I, IIA, and IIB, respectively) after bed rest (Table 1). The relative CSA occupied by type I fibers did not change (P = 0.64) after bed rest. The relative proportions of type I, IIA, and IIB MHC were 44.8 ± 12.2, 44.0 ± 17.8, and 12.6 ± 11.1% before bed rest, respectively. MHC composition was not altered (P = 0.79, 0.82, 0.73 for type I, IIA, and IIB, respectively) after bed rest (Table 1). There were high correlations between the type I fiber percentage and the relative proportion of type I MHC (r = 0.90; P < 0.05) and between the percentages of type IIA fiber and IIA MHC (r = 0.98; P < 0.05) classified from enzyme-histochemical myofibrillar ATPase stainings and by the use of SDS-PAGE (Fig. 3). There was no correlation between type IIB fiber and IIB MHC (r = 0.47; P = 0.29) percentages. The type IIB fiber percentage was higher (P < 0.05) than the relative proportion of type IIB myosin isoforms.
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Quadriceps muscle CSA. Quadriceps femoris CSA decreased (13.8 ± 4.5%; P < 0.05) from 76.7 ± 10.0 cm2 before to 65.8 ± 7.1 cm2 after bed rest. Peak torque per CSA decreased by 12.5 ± 9.5% (P < 0.05) after bed rest (Fig. 2).
DISCUSSION
The finding of a marked decline in maximum voluntary force after bed rest conforms with data from previous long-term unloading studies. The less severe, although manifest, muscle atrophy, as estimated in whole muscle or single muscle fibers, also agrees with previous reports. Neither fiber type composition nor in vivo force-velocity characteristics changed in response to bed rest. Because the decrease in muscle size alone cannot account for the reduced maximum voluntary force, it is concluded that a reduced neural input or reduced specific tension of muscle must, at least in part, be responsible for the large decrease in voluntary strength.
Maximum voluntary force decreased by 25-30% after 42 days of bed rest. This amounts to a decline of 4-5% per week. Previous data from experimental bed rest, lower limb unloading, or spaceflight ranging from 2 to 6 wk showed 12-21% strength loss of the knee extensors (2, 3, 11, 12, 18, 33). Studies of the human ankle extensors (18; cf. Ref. 10) also report changes of that magnitude in response to different unloading models.
The loss in muscular strength reported after unloading has mainly been attributed to a decrease in skeletal muscle mass. The muscle atrophy of 15% assessed in the knee extensors after 37 days of bed rest equals an average weekly decrease in muscle mass of ~3%. The majority of previous studies examining healthy individuals after 1-6 wk of unloading or bed rest (2, 3, 7, 9, 14, 20, 21) have demonstrated a similar (2-3%) weekly rate of atrophy in whole muscle or fiber CSA of the thigh or knee extensors. Three astronauts showed a 6% muscle atrophy in whole muscle CSA after 8 days of spaceflight (26). At odds with these reports, muscle fiber CSA decreased 11-36% in astronauts subjected to 5-11 days of weightlessness (13).
The greater loss in strength relative to the reduction in muscle CSA suggests specific tension of muscle and/or neural input to muscle is reduced. The observed changes in EMG activity support both the occurrence of diminished specific tension and thus decreased electromechanical efficiency of muscle and a reduced neural drive of the muscle. Recently, 10 days of lower limb unloading was shown to produce a significant strength loss but no decrease in maximum EMG activity (6), suggesting the knee extensor muscle to be less efficient in generating force per unit mass after short-term unloaded inactivity. The present results agree with those produced after short-term unloading, although there is a difference in the magnitude of response. Thus in both studies there was a marked increase in EMG intensity at a fixed submaximum load. A certain increase in EMG activity seems logical in light of the decrease in muscle mass because the atrophied muscle now has to produce a larger relative tension to attain the preset 100-Nm torque level. Support for this could also be found in a recent study (28) in which the exercise-induced contrast shift in MRI images of the knee extensors was quantitated before and after 5 wk of lower limb unloading. The atrophied quadriceps muscle showed increased contrast shift when producing a given amount of work after unloading, implying additional muscle fiber involvement after disuse. The increase in EMG amplitude in the present study far exceeded what would be expected from the decrease in muscle CSA. Because force per CSA of the knee extensors in fact decreased, as evidenced here during voluntary effort and as previously reported in maximally activated membrane-permeabilized single muscle cells in a subgroup of these individuals (24), the increase in submaximum EMG activity could be partly explained by a less efficient force generation. This, in turn, would demand increased neural input to attain the preset force. There was a significant, although less prominent, decrease in maximum EMG activity after bed rest, confirming the findings of others (11, 16, 19) suggesting decreased neural drive. These authors, however, did not report elevated EMG at submaximum effort. This may simply be explained by the readjustment of signal or target levels to the lower maximum capacity after disuse. Collectively, the results from this study suggest that the neural drive is indeed decreased after long-term bed rest but that there is a decreased electromechanical efficiency, as evidenced by increased EMG at a submaximum force, as well.
The demonstrated decrease in voluntary force per area in whole knee extensor muscle and of specific tension in single fibers (24) agrees with data obtained in hindlimb-suspended rats (8, 15, 17, 29, 34). Because contractile protein concentration was lowered in humans (24), similar to what has been reported in animals (8, 15), a decreased number of active cross bridges per volume of muscle after unloading may explain the loss in specific tension. This would, in turn, produce a decrease in electromechanical efficiency. Qualitative impairment in one or several of the other components in the contractile machinery (cf. Ref. 6) could, however, not be ruled out.
Animal data suggest that slow-twitch fibers are more vulnerable to unloading. Thus fiber type conversion and greater relative atrophy in predominantly slow than in fast muscles have frequently been reported (cf. Ref. 30). Slow fibers, but not fast fibers, also show a reduction in specific tension (cf. Ref. 17). No alteration in fiber type was shown in enzyme-histochemical assessments or in the relative proportion of MHC assessed in the same serial sections. Because of the high correlation between fiber type percentage and MHC composition assessed electrophoretically, shown here and previously (1, 31), a fiber type transformation in response to 37 days bed rest seems unlikely. Nor do the present results suggest a fiber type-specific atrophy that could potentially change the relative CSA occupied by a certain fiber type. Not only fiber type but also the relative fiber size influences specific MHC content. Hence unaltered MHC proportions across fibers allude to a uniform decrease of all MHC isoforms in the muscle. The decrease in specific tension of single fibers did not indicate differences among fiber types (24). Thus no qualitative changes in MHC or fiber type or the relative contribution of fast or slow muscle to knee extensor CSA seems to occur in response to bed rest. This response seems different from what occurs in lower mammals and, equally important, it would not significantly alter muscle function.
Force-velocity characteristics of the knee extensor muscle group did not show any alterations after bed rest. However, animal studies of whole muscle preparations (15) or single slow fibers (17, 29) have consistently reported an increased maximum velocity of unloaded shortening (Vo) after unloading. These changes are consistant with the finding that unloading appears to promote an increase in fast MHC isoform content in rat soleus muscle. Vo in single human fibers was unchanged when averaged for all fiber types of the quadriceps muscle after bed rest (24). In a consideration of previous human data, and because no changes in fiber type composition or MHC content occurred after bed rest, the finding of no increase in Vo is not surprising. It is noteworthy that the increased Vo demonstrated in rats occurred in parallel with fiber type transformation. The appearance of transformed fibers in fiber pools being analyzed constitutes a problem when the impact of unloading on a certain fiber type is being determined. In support of the lack of increase in single-fiber Vo in the subgroup examined in the parallel study (24), there was no increase in knee AVmax. In fact, a small (5%) decrease was demonstrated. This effect might be explained by decreased neural drive after bed rest. The force-velocity curve assessed during isokinetic knee extensions at selected angular velocities was not altered after bed rest. A similar lack of change has been reported elsewhere after unloading (2, 3, 11, 12). Because fast-myosin content, i.e., type II fiber percentage, has been correlated to knee extensor torque at higher velocities (cf. Ref. 32), the unchanged MHC and fiber composition support the unaltered in vivo force-velocity relationship reported here.
The present changes in muscle fiber size were similar when measured by using planimetry or calculated by using the smallest ellipse diameter in serial sections from biopsy samples, and the overall decrease paralleled the change in knee extensor CSA from whole muscle imaging. Because the interindividual variation in CSA was greater in fiber assessments than with the use of MRI, it might be anticipated that this variation does not illustrate individual differences in the atrophic response to bed rest only but rather that the inherent sampling error of the biopsy technique (2) is greater than that associated with MRI methodology (2, 26). It should be recalled, however, that tomographic CSA typically does not discern extracellular or other noncontractile components that contribute to the measured area. It is a matter for speculation whether swelling or fluid shift (5, 22) is altered in response to unloading and whether this could affect fiber or whole muscle CSA measurements at rest or after muscle use.
This study cannot explain the recurrent differences between human and animal data. Among the plausible explanations are species differences between lower mammals and humans, e.g., growth rate, fiber type characteristics, anatomy, and function. Because animal muscles are largely homogenous in fiber type, specific adaptation of different muscles may be regarded as synonymous with adaptation of different fiber types, when, in fact, there may be large differences also in anatomy and function. It could be noted that data that compare shortening velocity and specific tension in single fibers of different types in the same muscle are still lacking. On the other hand, this could imply that human data from the heterogenous knee extensor muscle may not be applied to the slow-twitch soleus and vice versa.
We conclude that the impaired musculoskeletal function reported here and elsewhere in response to unloading cannot entirely be attributed to muscle atrophy. Our data suggest that decreased neural drive and reduced electromechanical efficiency of skeletal muscle are responsible, in part, for a decrease in voluntary strength. Results also suggest that unloading produces no major changes in contractile properties or in fiber type or myosin composition of a heterogenous human muscle, implying that the response in humans differs from that seen in lower mammals.
ACKNOWLEDGEMENTS
Drs. Christian Denis and Dominique Desplanches, Departments of Physiology, St. Etienne and Lyon, France, respectively, are acknowledged for collaboration during sampling and preparation of biopsy specimens. Ulrika Müller, Department of Clinical Neurophysiology, Karolinska Hospital, is acknowledged for excellent electrophoretic separation and enzyme-histochemical stainings. Drs. P. Levorch, R. Aziza, and A. Maillet, Departments of Rehabilitation and Radiology/MRI, Rangueil University Hospital, and Institute de Médecine et de Physiologie Spatiales, Toulouse, France, respectively, are acknowleged for assistance and collaboration during data collection, processing, and transfer.
FOOTNOTES
Address for reprint requests: H. Berg, Dept. of Physiology and Pharmacology, Karolinska Institutet, S-171 77 Stockholm, Sweden.
Received 1 May 1996; accepted in final form 12 September 1996.
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B. C. Clark, B. Fernhall, and L. L. Ploutz-Snyder Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy J Appl Physiol, July 1, 2006; 101(1): 256 - 263. [Abstract] [Full Text] [PDF]
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B. C. Clark, T. M. Manini, S. J. Bolanowski, and L. L. Ploutz-Snyder Adaptations in human neuromuscular function following prolonged unweighting: II. Neurological properties and motor imagery efficacy J Appl Physiol, July 1, 2006; 101(1): 264 - 272. [Abstract] [Full Text] [PDF]
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B. Cormery, E. Beaumont, K. Csukly, and P. Gardiner Hindlimb unweighting for 2 weeks alters physiological properties of rat hindlimb motoneurones J. Physiol., November 1, 2005; 568(3): 841 - 850. [Abstract] [Full Text] [PDF]
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M. W. P. Bleeker, P. C. E. De Groot, G. A. Rongen, J. Rittweger, D. Felsenberg, P. Smits, and M. T. E. Hopman Vascular adaptation to deconditioning and the effect of an exercise countermeasure: results of the Berlin Bed Rest study J Appl Physiol, October 1, 2005; 99(4): 1293 - 1300. [Abstract] [Full Text] [PDF]
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N. Yasuda, E. I. Glover, S. M. Phillips, R. J. Isfort, and M. A. Tarnopolsky Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization J Appl Physiol, September 1, 2005; 99(3): 1085 - 1092. [Abstract] [Full Text] [PDF]
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N. D. Reeves, C. N. Maganaris, G. Ferretti, and M. V. Narici Influence of 90-day simulated microgravity on human tendon mechanical properties and the effect of resistive countermeasures J Appl Physiol, June 1, 2005; 98(6): 2278 - 2286. [Abstract] [Full Text] [PDF]
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P. A. Tesch, J. T. Trieschmann, and A. Ekberg Hypertrophy of chronically unloaded muscle subjected to resistance exercise J Appl Physiol, April 1, 2004; 96(4): 1451 - 1458. [Abstract] [Full Text] [PDF]
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G. R. Adams, V. J. Caiozzo, and K. M. Baldwin Skeletal muscle unweighting: spaceflight and ground-based models J Appl Physiol, December 1, 2003; 95(6): 2185 - 2201. [Abstract] [Full Text] [PDF]
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W D-C Man, M G G Soliman, D Nikoletou, M L Harris, G F Rafferty, N Mustfa, M I Polkey, and J Moxham Non-volitional assessment of skeletal muscle strength in patients with chronic obstructive pulmonary disease Thorax, August 1, 2003; 58(8): 665 - 669. [Abstract] [Full Text] [PDF]
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R. J. Talmadge, M. J. Castro, D. F. Apple Jr., and G. A. Dudley Phenotypic adaptations in human muscle fibers 6 and 24 wk after spinal cord injury J Appl Physiol, January 1, 2002; 92(1): 147 - 154. [Abstract] [Full Text] [PDF]
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S. W. Trappe, T. A. Trappe, G. A. Lee, J. J. Widrick, D. L. Costill, and R. H. Fitts Comparison of a space shuttle flight (STS-78) and bed rest on human muscle function J Appl Physiol, July 1, 2001; 91(1): 57 - 64. [Abstract] [Full Text] [PDF]
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G. Ferretti, H. E. Berg, A. E. Minetti, C. Moia, S. Rampichini, and M. V. Narici Maximal instantaneous muscular power after prolonged bed rest in humans J Appl Physiol, February 1, 2001; 90(2): 431 - 435. [Abstract] [Full Text] [PDF]
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K. Michael Relationship of Skeletal Muscle Atrophy to Functional Status: A Systematic Research Review Biol Res Nurs, October 1, 2000; 2(2): 117 - 131. [Abstract] [PDF]
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D. L. Williamson, M. P. Godard, D. A. Porter, D. L. Costill, and S. W. Trappe Progressive resistance training reduces myosin heavy |
ABSTRACT