Decreased use, exposure to microgravity, and limb immobilization all result in loss of muscle mass that impairs functional capacity and may compromise health. Loss of skeletal muscle strength and endurance diminishes capacity for independent living in older adults and capacity for work during or after spaceflight in astronauts. Loss of muscle mass also is associated with decreased glucose tolerance (13), decreased resting metabolic rate (RMR) (28), and decreased bone mineral density (BMD) (19). Thus, muscle mass and function have many links to health and well-being, and it is important to identify factors that influence loss of muscle mass and function during periods of disuse or unloading.
Several research papers report large variability in the degree of muscle mass lost during unloading and immobilization (1,3,20). Akima et al. (1) measured muscle atrophy in three astronauts and found three- to fourfold variability in the amount of muscle loss after only 4 d of spaceflight. Similarly, changes ranged from −9.66 to 0.20% and −27.2 to −3.7% for forearm muscle atrophy after 9 and 21 d of immobilization, respectively (3,20). Clearly, some individuals are more prone than others to rapid muscle loss. Another point illustrated by these data is that the extent of muscle loss and the range of responses increase as the duration of disuse increases.
Factors associated with increased susceptibility to loss of muscle mass and function are not well known. Unloading-induced atrophy appears to be greater when initial muscle fiber cross-sectional area (CSA) is greater (7) and when muscles are held in a shortened position (4). However, little is known about the level of use the muscle is accustomed to before disuse. Will resistance exercise render muscle more or less resistant to atrophy during disuse? One study of resistance training before thenar muscle immobilization suggests that there may be a protective effect (25). The answer to this question may help individuals who can anticipate muscle disuse, for instance, spaceflight or orthopedic surgery, and may help to promote resistance training across the population as a prophylactic measure in case of injury, for instance, hip fractures in older adults.
In addition to the level of muscle use before unloading, potential sex-related differences in the response to unloading have not been sufficiently investigated. Sex differences are apparent in the loss of skeletal muscle mass with aging and in the endocrine response to resistance training (6,17). The identification of sex-specific training differences suggests that sex-specific detraining or disuse differences merit investigation. Further, women typically have been represented in disuse studies as a small proportion of the research population (5,8), and only a few studies have focused on women (9,14,15,20,30). Early studies comparing men and women in response to disuse suggest that there are sex differences in strength loss and atrophy, but sample sizes for women have been from four to seven subjects, and conclusions are difficult to draw (9,14,15,30).
Functional capacity also is important to health, for instance, ability to exercise, perform necessary tasks, and prevent falls. The factors that may protect an individual from loss of strength and muscle endurance during disuse may not be the same as those that protect against atrophy. Both atrophy and neural factors have a combined effect such that the proportion of strength lost typically is greater than the proportion of muscle CSA or volume that is lost (5,14,15,20,22). On a related note, it seems likely that disproportionate changes in muscle fiber CSA and neural activation may lead to errors in sense of muscular effort or force. However, this has yet to be investigated. Finally, several studies report increased fatigability of muscle after unloading (5,7,12).
Identification of the factors associated with an increased tendency for muscle atrophy and loss of neuromuscular function is important for understanding disease risk and prevention, as well as for the design of countermeasures to prevent atrophy during spaceflight or during recovery from injury. Thus, the purpose of this investigation was to determine whether 1) level of use (resistance training or not) before arm suspension and 2) sex differences influence the magnitude of muscle atrophy and functional changes in response to 21 d of skeletal muscle arm suspension. Based on previous research, we hypothesized that resistance training before arm suspension may protect from decreases in strength and endurance (25), and there may be sex-related factors that protect women from these same losses (15,30). However, there are few data available to predict whether protection against functional loss associated with resistance training or sex will be reflected in protection against atrophy.
Potential participants were screened for inclusion and exclusion criteria and gave written informed consent for the protocol approved by the human subjects committee at Montana State University before enrollment in this investigation. To be included, subjects must have been between the ages of 18 and 30 yr, not have participated in any resistance training or other regular strenuous activity using the upper body in the previous year, not have musculoskeletal conditions that would interfere with this investigation, and answer “no” to all questions on the Physical Activity Readiness Questionnaire (PARQ). Additionally, subjects were excluded if they did not meet the safety criteria for magnetic resonance image (MRI) procedures. A total of 36 subjects were enrolled in the investigation. Thirty-one subjects (18 women and 13 men) completed the investigation. Five subjects began the investigation but did not complete the investigation due to personal reasons or inability to comply with experimental procedures.
Subjects were assigned to one of two groups, balanced by sex, for a protocol consisting either of 8 wk of progressive resistance training followed by 21 d of arm suspension (TRAINED group), or only the 21 d of arm suspension (UNTRAINED group). The experimental design and time course for measurements are illustrated in Figure 1. Progressive resistance exercise in the TRAINED group targeted the elbow flexor muscles. The arm suspension protocol for both groups consisted of wearing a sling and swathe that restricted used of the shoulder, elbow, and hand. Criterion measurements included brachial circumference, maximal isometric force (MIF), one-repetition maximum (1RM) biceps curl strength, elbow flexor muscular endurance, sense of muscular effort, and muscle volume measured using MRI. The arm suspension procedure was applied to the nondominant arm, and the contralateral arm was designated as a normal use control arm for brachial circumference, MIF, sense of muscular effort, and muscle volume.
Progressive resistance exercise training.
Progressive resistance training was performed for the elbow flexor muscles of both arms. The training occurred during the 8 wk preceding the arm suspension and ceased for both arms 48 h before and during the arm suspension protocol. Exercises included biceps curl with supination (from pronated and extended to flexed and supinated) and biceps crunches (from an enclosed elbow angle of just over 1.57 rad to full flexion). Training began at three sets of 12 repetitions at 50–60% of 1RM and progressed to three sets of eight repetitions at 80–90% of pretraining 1RM by the final 2 wk of training. If subjects were able to complete all repetitions within a workout, resistance was increased by 2.3 kg at the next workout.
Arm suspension of the elbow.
Subjects wore a sling to suspend the elbow in a flexed position (approximately 1.57 rad) and a swathe to hold the arm in the sling against the torso. Thus, this treatment resulted in suspension and a substantial degree of immobilization. The sling unloaded the elbow flexor and extensor muscles while the swathe relieved the shoulder muscles of the need to support the arm. This is a modification of the model proposed by Parcell et al. (22) to simulate weightlessness. The sling and swathe (Joslin Orthopedic Gear, Brisbane, CA) were worn at all times during waking hours except during bathing. The arm was free during sleeping.
A spring-loaded anthropometric tape measure was used to measure the upper arm circumference at the midbrachial point of both arms. Three ink dots were used to mark the location of the measurement and were maintained from pre- to postdisuse measurements. This measure was used as a gross determination of potential muscle hypertrophy in response to progressive resistance training for the TRAINED group because we were unable to include a pretraining MRI.
Strength of the elbow flexor muscles was determined through a MIF measurement and determination of 1RM for the biceps curl. Maximal isometric force measurements were made with subjects seated at a preacher curl bench with an enclosed elbow angle of 1.57 rad (90°). A handle connected to a Chatillon CSD500 load cell (Ametek TCI, Largo, FL) was tethered to a moveable floor mount and positioned such that the angle formed by the forearm and strain gauge cable also was 1.57 rad. Settings were recorded so that the identical setup could be replicated for measurements on all days. Three repetitions of 5-s duration were performed for each arm with 1 min of rest between repetitions. Determination of 1RM for the biceps curl of each arm was performed separately using progressive trials with dumbbell free weights.
Sense of muscular effort.
Sense of muscular effort between the arm suspension and control arms was measured using a force-matching test (23,24,26). After the measurement of MIF, a second load cell (model 465, Omega Engineering, Stamford, CT) with an identical set up was put in place so that force output from each arm could be measured simultaneously. The load cell was attached to a strain gauge amplifier, and the analog output was converted to digital output and recorded using LabVIEW software (version 5.1, National Instruments, Austin, TX). LabVIEW software was used to generate a visual target on the computer monitor of 30% of MIF measured for the suspended arm. On cue, subjects generated what they felt was equal force with both arms until the target force was reached by the control arm. The force of the suspension arm was unknown to the subject. Subjects gave a verbal cue to indicate when they felt they were generating equal force with both arms, and investigators initiated measurement of the force produced by the suspended arm.
Data were analyzed by determining variable and constant error scores from the raw data (26). Variable error is the amount of variation (standard deviation) around the mean score for multiple trials or the consistency of the test. Constant error is the mean score of overshooting or undershooting across multiple trials, that is, mean distance from the target. Thus, a systematic change in constant error would indicate that arm suspension influences sense of force (26). Both types of error were calculated in relative units (%).
A muscular endurance test for the elbow flexor muscles was performed only for the suspended arm. For this test, subjects performed concentric biceps curls using 50% of their current 1RM at a rate of one repetition per 2 s. To avoid muscle soreness induced by eccentric muscle activity, the weight was lowered by an investigator. Subjects performed repetitions until they could not keep the pace or they reached 100 repetitions.
Serial muscle CSAs measured using 1.5-T, T1-weighted MRI (Marconi Eclipse, Philips Medical, Cleveland, OH) were used to calculate volume of the flexor and extensor muscles, respectively. A body wrap coil was positioned around one arm of the subject in a supine position on the conveyor of the MRI. Locator scans were used to locate a radiological marker placed at the midbiceps level, and then a series of images of 3.0-mm width, with 0.5 mm between were collected. The image containing the marker was identified and filmed along with the images 10.5 and 21.0 mm proximal and distal to that point. This procedure was repeated for the contralateral arm.
The outline of the flexor muscles (m. brachialis and m. biceps brachii) from the films was traced by a single investigator. Five traced images from each arm (10.5 and 21.0 mm above and below the midbiceps) were converted to JPEG files using a scanner and muscle areas in centimeters squared were digitized using Scion Image software beta 4.02 (Scion Corporation, Frederick, MD). Each image was digitized in duplicate (average area used for analysis) and all images from an individual subject were digitized by the same investigator. Muscle volumes between adjacent muscle areas 10.5 mm apart were calculated using the following formula for the volume of a frustum (base of a cone): V = (π·h·1/3) (r12 + r1r2 + r22) where V = volume, h = 0.105-cm height, and r1 and r2 = the radii of the adjacent muscle areas. The muscle volume was the sum of the four frusta measured for the flexor muscles. The average intrasubject coefficient of variation from pre- to postdisuse for this procedure calculated using the bone volume attained from the same images and the described procedures was ±2.80%.
Statistical analyses were performed using Statistica version 6.0 software (StatSoft, Inc., Tulsa, OK). Descriptive data are presented as mean ± standard deviation. Data were tested for normal distribution using the Shapiro–Wilk W test and transformed to meet the normal distribution if necessary. Transformed variables included MIF, number of repetitions to fatigue, and variable error within the force proprioception test. Repeated measures ANOVA with main effects for arm suspension (average of the two predisuse vs postdisuse), group (TRAINED vs UNTRAINED), sex (men vs women), and where appropriate, arm (arm suspension vs normal use control) was used to identify the effects of arm suspension and the influence of training and sex on the magnitude of the response. Tukey post hoc comparisons were used to locate differences between means when significant interactions were identified. Pearson product–moment correlation coefficients were calculated to determine the relationship between muscle volume and strength parameters.
Effects of progressive resistance training.
The TRAINED group responded to the progressive resistance exercise with increased (P < 0.001) MIF (14.9 ± 12.1 N) and 1RM (6.5 ± 4.5 kg). Although training did not impact the number of repetitions completed at 50% of 1RM for the muscular endurance test, the posttraining resistance was greater than that used pretraining because of the increase in 1RM.
With respect to a potential hypertrophy response to resistance training, there was an increase (P < 0.01) in midbrachial arm circumference when data from men and women were collapsed together. When examined specific to sex, women tended to have a greater increase (sex by training interaction P = 0.06) in circumference compared with men (1.0 ± 0.8 cm) compared with men (0.4 ± 0.5 cm).
Presuspension descriptive data.
Thirty-one subjects completed the investigation. The TRAINED (N = 15) and UNTRAINED (N = 16) groups were similar within each sex for age, stature, mass, isometric force, and endurance of the elbow flexor muscles (Table 1). Main effects for sex were identified in which men were greater (P < 0.05) than women in stature, brachial circumference, MIF, and 1RM. Before progressive resistance exercise, the TRAINED and UNTRAINED groups did not differ in MIF production for elbow flexion at 1.57 rad, and the UNTRAINED group was higher (P < 0.05) than the TRAINED group for 1RM of the biceps curl.
Data from one woman was excluded from this portion of the analysis owing to an error in the MRI procedure. Flexor muscle volume was greater (P < 0.001) for men compared with women both pre- and postdisuse. Elbow flexor muscle volume of the suspended arm decreased by −7.7 ± 7.3% from pre- to postdisuse. However, there was a disuse treatment by sex interaction (P < 0.001), and post hoc analysis identified a decrease (P < 0.001) in flexor muscle volume in men but not in women (Table 2).
Both MIF and 1RM declined (P < 0.001) following arm suspension (Figs. 2 and 3). Interactions between the arm suspension treatment and either sex or training group were of particular interest, but neither was significant for MIF or 1RM. That is, the decrease in both isometric force and 1RM was similar in the TRAINED and UNTRAINED groups (Figs. 2 and 3). Men were stronger (P < 0.001) than women at all time points for both 1RM and MIF, but the loss of strength during arm suspension was similar in both sexes.
Muscle volume and force relationships.
The ratio of MIF to flexor muscle volume decreased (P < 0.05) from pre- to postdisuse in women but not in men (Fig. 4). Effects of training group were not detected. The relationship between volume and force appeared to be stronger in men (r = 0.70 and 0.80 pre- and postdisuse) than in women (r = 0.45 and 0.26 pre- and postdisuse).
The number of repetitions to fatigue at 50% of 1RM was greater (P < 0.01) in women compared with men and greater (P < 0.05) in the TRAINED compared with the UNTRAINED group both before and after arm suspension. Following disuse, it was determined that the number of repetitions at 50% of 1RM decreased (P < 0.05) in the UNTRAINED group, but not in the TRAINED group (Fig. 5).
Sense of muscular effort.
Force-matching error scores did not change over the course of the investigation, and no differences were detected between training groups. There was a significant disuse treatment by sex interaction (P < 0.05) for variable error (standard deviation of three error scores for repeated trials in a given day). Post hoc analysis indicated that variable error increased pre- to postdisuse in men, but not in women (Table 3). Constant error scores did not change over time, and there were no differences between groups. These data suggest that while there was more variability in force-matching accuracy by men following arm suspension (variable error), the tendency to systematically over- or undershoot the target force (constant error) was not influenced by the arm suspension protocol or group.
The experimental model of arm suspension of one arm employed in this investigation induced changes in muscle volume, strength, and endurance. The key findings of this investigation were that resistance training before arm suspension attenuated loss of endurance, but had no impact on the relative loss of muscle volume and strength. Secondly, while there were no sex differences in the relative loss of muscle strength and endurance, a greater atrophy response was measured in men compared with women. An additional unique finding of this investigation was that sense of muscular effort did not appear to be altered by the loss of muscle volume or strength.
The majority of work related to disuse from immobilization, suspension, bed rest, and spaceflight has focused on the lower limb because of its antigravity and weight bearing roles (1,2,3,4,5,8,14,15,27,29) compared with the upper limb (12,20,22), despite its role in lifting and manipulating objects. The decreases we measured in muscle volume (−2.6%·wk−1) and strength (about 4–5%·wk−1) of the arm are comparable to many of the studies focusing on leg muscles, suggesting that more attention to changes in the upper body may be warranted.
Influence of resistance training before arm suspension.
Eight weeks of progressive resistance training before arm suspension did not influence the relative magnitude of muscle loss. One weakness of this study is that we were unable to measure muscle volume before resistance training in the TRAINED group; therefore, it cannot be determined whether the training protocol induced hypertrophy. The classic work of Moritani and deVries (21) established that the gains in strength at the onset of resistance training result from neural factors and that hypertrophy becomes the dominant factor in strength gain after 3–5 wk of training. This time course, in conjunction with the measured increase in brachial circumference after 8 wk of resistance training, suggest that hypertrophy may have occurred in the TRAINED group before the arm suspension treatment. Similar relative decreases in TRAINED and UNTRAINED groups suggest that neither increased muscle activity nor potential gains in muscle volume before disuse influenced the rate of muscle loss. Other studies have found that resistance training countermeasures during disuse are effective in preventing muscle atrophy (2,14,27,29). Therefore, we conclude that gaining muscle mass before arm suspension is likely to be advantageous, but preventing atrophy requires countermeasures during disuse.
Strength gains from resistance training also may be advantageous because losses in MIF and 1RM were similar in TRAINED and UNTRAINED groups. Sale et al. (25) found that the relative strength decrease in thenar muscles after 18 wk of immobilization was lower in a preimmobilization resistance trained group compared with an untrained group. The enhanced protection measured in the study of Sale et al. (25) compared with the present study may be a function of measuring muscles with different types and levels of functional use, or perhaps, the effect of resistance training before unloading is greater when the duration of unloading is longer than in the present investigation.
In the present study, an endurance test was performed at 50% of the current 1RM, and there was a decrease in repetitions to fatigue following arm suspension in the UNTRAINED, but not TRAINED, group. This is consistent with previous studies reporting similar rates of fatigue but lower total work or isometric force over time in untrained subjects. These studies also adjusted workloads to pre- and postdisuse strength levels (12,20). Thus, resistance training before spaceflight or orthopedic surgery may provide endurance benefits for postflight or postsurgical muscular endurance.
If we consider endurance from the perspective of work performed, then we may infer from our data (same number of repetitions with a lower weight) that endurance decreased in all groups. This finding has been reported in other research studies of both the lower and upper limbs (5,12). Research into the energy producing capacity of muscles suggests that decreases in mitochondrial enzymes and oxidative capacity following immobilization occur (4,12). However, at least one study measured no change in oxidative and glycolytic enzyme concentrations after 17 d of spaceflight or bed rest (29), suggesting that nonmetabolic factors may influence endurance after disuse.
We compared responses of men and women to determine whether sex-specific factors influence the extent of atrophy occurring in response to arm suspension. Men lost about 10% of elbow flexor muscle volume compared with a nonsignificant loss in women. Similarly, Yamamoto et al. (30) reported greater decreases in leg muscle mass for men (5.2%) compared with women (3.3%) after 20 d of bed rest. Estrogen is a potential factor differentiating women and men, but it did not protect against muscle loss during hindlimb suspension in rats (11). Another difference between the sexes in the current study is the larger initial muscle volume in men compared with women. Fitts et al. (7) suggested that one factor enhancing the degree of atrophy may be a greater initial muscle CSA. This suggests that muscle size rather than endocrine factors influence sex-specific muscle preservation in women, but further research is needed to clarify this mechanism.
Relative losses in endurance and strength were similar in men and women. Although women performed their endurance tests with a lower absolute mass, they were able to perform more repetitions before fatiguing. Both MIF and 1RM values for the women were roughly 50–60% of those for the men before and after disuse, and this is consistent with the expected sex difference for strength in the upper body (16). Koryak (15) measured 1.3- to 3.2-fold greater relative losses in isometric and tetanic twitch tensions and maximal voluntary contraction forces of the triceps surae in six men compared with four women after 120 d of head-down bed rest. However, Yamamoto et al. (30), in agreement with our findings, measured similar percent decreases in men and women after 20 d of bed rest. It may be that women fare better than men as the duration of disuse gets longer, or that the nonweight-bearing upper body and weight-bearing lower body muscles respond differently. More research with longer durations of disuse and larger sample sizes appears warranted.
We found that the force to muscle volume ratio decreased in women but not men after 21 d of arm suspension. That is, we found that strength decreased in women despite a nonsignificant change in muscle volume. Koryak (15) measured a larger difference between electrically stimulated tetanic contraction force and maximal voluntary force (force deficiency) in women compared with men before bed rest; however, the force deficiency had increased more dramatically in men compared with women after 120 d of bed rest. This prompted Koryak to suggest, in contrast to our findings, that losses in neural activation were less marked in women compared with men in response to unloading. One difference between our work and that of Koryak is the measurement of upper and lower limbs, respectively. Additional research to address this issue is needed.
Sense of muscular effort.
The ability of our subjects to estimate the effort produced by the suspended arm, in matching it to 30% of its MIF for that testing session held by the control arm, did not change systematically with arm suspension. Sense of muscular effort and force is derived from both central perception of effort and peripheral feedback from afferent receptors, most notably the Golgi tendon organs that provide peripheral feedback regarding changes in muscle tension (23). Sense of effort is appropriately assessed using a force-matching task across contralateral limbs (23). Perturbations to skeletal muscle such as fatigue and exercise-induced muscle damage have been shown to alter sense of effort such that individuals systematically overestimate force production (24,26). Further, changes in the Golgi tendon organ have been measured after tenotomy, immobilization, and spaceflight (10,18). As force matching was a static task (23), we conclude that the loss of strength did not disrupt central perception of effort and force production.
Both the level of activity before arm suspension and the sex of the individual influenced the response to arm suspension of the elbow flexor muscles. Benefits of resistance training before disuse include maintaining a higher strength level and attenuation of loss in muscular endurance. The smaller initial muscle size or sex-specific factors attenuated muscle loss but not strength loss in women during disuse.
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