Reduced skeletal muscle contractile strength is a well-established adaptation to unloading and is amplified in weight-bearing extensor muscles(14,17,30). Because of its important function during both standing posture and locomotion, the plantar flexor muscle group has received much attention in studies of reduced loading(17,19,26,27,30,31). Losses in plantar flexor strength during ground-based unloading range 17-26% after 5-17 wk (17,31). This marked and rapid strength loss must be prevented if astronauts returning from extended duration space flights are to safely egress the Orbiter and return to ambulatory function in terrestrial gravity. Maintenance of plantar flexor strength in bedridden hospital patients is also vital for preserving ambulatory mobility on discharge.
Mechanical overload associated with resistance training enhances plantar flexor strength during normal weight-bearing (33) and has been recommended for space flight as a countermeasure against unloading-induced strength loss (2,15). Use of resistance exercise during bed rest unloading (BRU) has been limited to two studies (16,18). In both studies, frequent (5-6 d·wk-1) concentric isokinetic (18) or concentric isokinetic combined with isometric (16) exercise attenuated loss of knee extensor strength specific to the mode of training, but eccentric strength and alternate test modes were not evaluated. It is generally thought that a countermeasure to space flight atrophy should include eccentric contractions (2,15). Critical to the understanding of the effects of resistance exercise is a description of the training stimulus employed. Volume, load, frequency, and rest intervals are important determinants of training adaptations. In ambulatory subjects, improvements in strength, muscle mass, and neural drive are consistently found after training 2-3 d·wk-1 for 10-20 wk at 75-85% of concentric one-repetition maximum (1RM)(12,15,25,28,29,32). Greater training adaptations are found when at least 50% of the work is eccentric (15,20,22,25). We hypothesized that a similar resistance training regimen would protect plantar flexor performance during BRU. Thus, the purpose of this study was to test the efficacy of plantar flexor concentric/eccentric constant resistance exercise against the effects of BRU on strength performance. To gain a better understanding of bed rest deconditioning and the impact of our countermeasure, a comprehensive assessment of strength was conducted. Several contractile modes and velocities were tested including constant resistance 1RM, isokinetic torque-velocity, power-velocity, and torque-position relationships, and contractile work capacity. In addition, we assessed neural activation during static contractions since some have indicated unloading-induced strength loss is partially caused by reduced neural drive(9,13).
METHODS
Subjects. Sixteen healthy men were recruited from the greater Houston (TX) metropolitan area and were randomly assigned to no exercise (NOE,N = 8) or resistance exercise (REX, N = 8). Subjects were normotensive, nonsmoking, and passed a comprehensive physical examination including a diagnostic stress test. To ensure that the effects of BRU were studied exclusive of the effects of detraining, only individuals who had not participated in a resistance training program for at least 1 yr before the start of the study were allowed to participate. All subjects were given an oral and written briefing before signing informed consent. Subjects were housed in the General Clinical Research Center (GCRC) at The University of Texas Medical Branch-Galveston for 16 d (1 ambulatory, 14 bed rest, 1 recovery). The protocol was approved by the Institutional Review Boards of NASA Johnson Space Center and The University of Texas Medical Branch-Galveston.
Bed rest procedures. Subjects were fed an isocaloric diet with protein consumption maintained near 1.1 g·kg-1. Body weight was assessed daily via a bed scale. Subjects remained in a 6° head-down tilt at all times throughout BRU except during defecation (a commode chair was placed next to the bed) and for 30 min every other day during either supine resistance training (REX) or supine out-of-room rest (NOE). Subjects did not undergo any weight-bearing posture during transfer from head-down tilt to either the commode chair or the training device during the 14 d. All strength tests were conducted before reambulation.
Resistance training. Training consisted of constant resistance concentric/eccentric plantar flexion exercise every other day during BRU from the supine position using a horizontal leg training device (Cybex Strength Systems, Ronkonkoma, NY). Subjects performed five sets of 6-10 repetitions, taking each set to volitional fatigue. Loads were continuously adjusted to induce failure within the desired repetition range, thus progression was always incorporated into the program. Rest between sets was limited to 90-120 s. The load for a single warm-up set was two-thirds of the previous training session's eight repetition maximum (8RM).
1RM strength. One repetition maximum (1RM) plantar flexion strength was tested using the supine training device. Following sufficient warm-up, sets of one repetition were executed with increasing resistance up to two failed attempts at a given load. The greatest load lifted successfully was the 1RM. Trials were separated by 2-3 min. The range of motion was standardized for each subject and repeated post-BRU. One familiarization session preceded all strength testing. 1RM strength of two REX subjects exceeded the maximum load for the device (300 kg); thus N = 6 for REX 1RM results.
Torque-velocity relationship. The in vivo torque-velocity relationship was tested as described by Dudley et al.(14) with modifications for the plantar flexors. Unilateral angle-specific (1.57 rad) torque was determined across five velocities (0, 0.52, 1.05, 1.75, and 2.97 rad·s-1) on an isokinetic dynamometer (LIDO, Loredan Biomedical, Inc., Davis, CA) using the dominant leg. The neutral angle of 1.57 rad (90°) was selected to ensure a constant angular velocity before the test angle(14,34). For each dynamic velocity, three maximal effort repetitions were performed with concentric and eccentric phases separated by a 2-s pause. Range of motion for all subjects exceeded 0.96 rad(55°), with a minimum of 0.38 rad (22°) dorsiflexion and 0.57 rad(33°) plantar flexion relative to the neutral angle of 1.57 rad. Rest periods of 2-3 min were given between velocity tests. Dynamometer positions for each subject were recorded during pre-testing and repeated at post-testing. Subjects performed 15 submaximal warm-up contractions at 1.05 rad·s-1 before maximal tests. Velocities were tested in random order before BRU and the same order was repeated after BRU. Concentric and eccentric repetitions yielding the greatest angle-specific torques were selected for analysis. Peak angle-specific isometric torque was determined from three 4-s maximal voluntary contractions (MVC). Subjects were instructed to contract with maximal effort and as rapidly as possible. Contractions were separated by 2-3 min to prevent fatigue (35). The isometric test protocol was repeated for dorsiflexion.
Power-velocity relationship. Power-velocity relationships were derived from data collected during torquevelocity testing. For each of the four dynamic velocities, the repetitions yielding the highest concentric and eccentric work (J) outputs within a specified range of motion were selected. Work performed between 0.35 rad (20°) dorsiflexion and 0.52 rad (30°) plantar flexion was used to calculate power in W. This method standardized the range of motion across all subjects and all velocities and excluded artifact at the range of motion extremes.
Torque-position relationship. Concentric and eccentric torque-position relationships were determined at the slow velocity (0.52 rad·s-1). The range of motion analyzed was standardized across all subjects as described above. Torques were averaged every 0.14 rad (8°) to construct curves with six discrete points. Curves were then divided into three regions identified as stretched (dorsiflexed), neutral, and shortened(plantar flexed) muscle lengths. The two points in each region were averaged for statistical analysis but are displayed individually to maintain curve shapes.
Contractile work capacity. Contractile work capacity was assessed during a unilateral 10-repetition protocol performed at an angular velocity of 1.05 rad·s-1. The concentric and eccentric phases of each repetition were separated by a 2-s pause. Subjects were instructed to exert maximal effort during each repetition. Concentric and eccentric total work across ten repetitions were analyzed separately.
Neural activation. Electromyographic activity (EMG) was recorded from medial gastrocnemius, soleus, and tibialis anterior during MVC with pre-amplified bipolar skin surface electrodes (silver/silver chloride, 8 mm diameter, fixed interelectrode center distance of 19 mm) following procedures we have described previously (5). To ensure the same electrode position after BRU, sites were marked with ink during pretesting and maintained throughout BRU by the GCRC nursing staff and the investigators. The trial displaying the greatest torque was selected for EMG analysis. The root-mean-square (RMS) value was computed from raw data for each muscle using standard calculations. RMS was averaged over 1000 ms centered about peak torque. Gastrocenemius and soleus RMS values were averaged to represent plantar flexor activity.
Data analysis. All group scores on dependent variables are reported as the mean and its SE. Main effects of time and group by time interactions for most variables were tested by 2(group) × 2(time) ANOVA. Pre- to post-BRU differences within groups were tested by means comparisons. Torque-position relationships were analyzed by 2(group) × 3(position)× 2(time) ANOVA. For torque-velocity and power-velocity relationships, effect of concentric velocity on change in performance in NOE was tested by 4(velocity) × 2(time) ANOVA and effect of mode (concentric or eccentric) was tested by 2(mode) × 2(time) ANOVA. Significance was accepted at aP < 0.05 level of confidence.
RESULTS
Subjects. Subject characteristics by group are presented inTable 1. No group differences were noted in age, height, or weight. Body weight did not change during BRU. Isokinetic testing was introduced after the first group of four subjects (2 NOE, 2 REX) completed bed rest; thus N = 6 per group for all isokinetic test data.
1RM strength. 1RM heel raise data are shown inTable 2. A group by time interaction was found(P < 0.05) and 1RM was reduced 9.3% in NOE and improved 10.8% in REX.
Torque-velocity relationship. The angle-specific torque-velocity relationship is shown in Figure 1. No significant changes in torque were found in REX across all eccentric, isometric, and concentric velocities. Main effects of time were noted at isometric and slow concentric(0.52 and 1.05 rad·s-1) velocities (P < 0.05). Within groups, angle-specific torque at these three test velocities was reduced only in NOE, 12.9%, 18.2%, and 16.8%, respectively. Eccentric group by time interactions were found at 0.52 and 2.97 rad·s-1, with reductions in NOE of 20.2% and 13.0%, respectively (P < 0.05). Groups were different at three of four eccentric velocities (0.52, 1.05, 1.75 rad·s-1), with REX displaying greater torques. No velocity by time or mode by time interactions were noted in NOE.
Power-velocity relationship. Concentric and eccentric power-velocity relationships are displayed in Table 3. Power production in REX did not change after BRU. Interaction and time effects were found for concentric power at 1.05 rad·s-1. NOE concentric power at 0.52 and 1.05 rad·s-1 fell 15.9% and 26.3%, respectively. Interactions for eccentric power were noted at 0.52, 1.05, and 2.97 rad·s-1, with reductions in NOE of 16.3%, 12.0%, and 12.8%, respectively. Groups were different at the slowest concentric and three of four eccentric velocities (0.52, 1.05, 1.75 rad·s-1), with REX displaying greater power.
Torque-position relationship. Concentric and eccentric torque-position relationships are shown in Figure 2. Curves were constructed from six discrete points in the range of motion and were then divided into three regions identified as stretched (dorsiflexed), neutral, and shortened (plantar flexed) muscle lengths. The two points in each region were averaged for statistical analysis but are displayed individually to maintain curve shapes. Group by time interaction was found for eccentric torque. REX did not lose torque at any joint position after BRU, and a 6.3% increase was found for REX during eccentric contraction in the dorsiflexed position. NOE lost both concentric and eccentric torque in the neutral and dorsiflexed positions (range 13.9-17.9%). Groups were found to be different, with torque by position greater in REX.
Contractile work capacity. Results from the 10-repetition protocol are shown in Table 2. An effect of time was noted for concentric work and an interaction was found for eccentric work. Within groups, reduced work was noted only in NOE (concentric 15.1%, eccentric 11.1%).
Neural activation. RMS EMG results are presented inTable 2. There were no changes in maximal plantar flexor RMS EMG in either group. Dorsiflexor maximal RMS EMG fell 12.3% in REX. No changes were noted in antagonist co-activation for either group during plantar flexion and dorsiflexion.
DISCUSSION
In this study, concentric/eccentric constant resistance exercise during BRU prevented loss of strength performance in all contractile modes tested. This finding was somewhat surprising since performance benefits of resistance training are often revealed only when testing occurs in the mode of training(3,12,32) or near the training velocity(6,10). For example, McCarthy et al.(32) report a 23% increase in constant resistance 1RM after 10 wk of constant resistance training but no improvement in isokinetic strength. We have previously found improvements in isokinetic strength (10%) after constant resistance training, but the gains were relatively small compared with 1RM strength gains (25%) (24). Clearly, the benefit of training in the present study was most pronounced in the 1RM(11% increase), but there was considerable carry-over to isokinetic and isometric testing since marked losses in NOE were completely ameliorated. The aim of the present study was to prevent bed rest-induced strength loss, not to improve strength. The increased 1RM suggests the training volume and/or frequency prescribed was probably more than the minimum necessary to maintain plantar flexor 1RM during unloading. This may, in part, explain the“training effect” in isokinetic and isometric actions. We have previously shown (knee extensors) that bed rest-induced strength reductions in alternate test modes persist if constant resistance training is sufficient only in maintaining 1RM (3,4).
The resistance training program in this study was designed to maximize muscle activation/loading in a minimal amount of time. Plantar flexor training sessions were completed within 10 min and occurred every other day. The results of this study are encouraging for space flight exercise prescription since minimizing crew time spent exercising is a high priority. Further, these data suggest that a rather low weekly volume of resistance exercise in the hospital may play a significant role in preventing the decline in post-discharge ambulatory function well documented among bed- or chair-bound patients (23). It is important to emphasize, however, that a key to the effectiveness of our training protocol was probably strict adherence to contraction intensity. Intensity exceeded 75% of 1RM which has been shown repeatedly to markedly enhance strength in ambulatory subjects(15,20,24,28,32).
An important finding from the present study was maintenance of contractile work capacity in REX in the face of a 13% loss seen in NOE. While maximal strength in single efforts provides valuable information related to peak strength performance, a more practical measure of a countermeasure's efficacy is probably its ability to prevent loss of performance across repeated muscle efforts. A contraction paradigm such as this more closely simulates in-flight work tasks since most tasks demand muscular endurance along with adequate strength. Maintenance of contractile work with only 10 min of high-intensity contractions every other day should have significant implications for space flight exercise countermeasures.
BRU has been shown to reduce plantar flexor concentric strength (at 1.05 rad·s-1) 17-26% after 5-17 wk(17,31). At the same test velocity we found a 17% reduction in concentric strength after only 2 wk of BRU (NOE group). Taken together, these data indicate a rapid time course for strength loss at the onset of unloading that appears to plateau with extended durations.
Several investigators have quantified changes in knee extensor strength during unloading by analyzing the in vivo torque-velocity relationship(1,3,8,9,13,14). An important feature of this technique is control of muscle length(10,34). This facilitates comparisons across contractile velocities and modes and offers a method by which direct comparisons can be made before and after an intervention. After 14-42 d, knee extensor anglespecific torque has been shown to decrease 12-26%(1,3,8,9,13,14). In these studies, the magnitude of strength loss was independent of contractile mode(concentric vs eccentric) or contractile velocity. We found similar results in the plantar flexor muscle group; there were no mode by time or velocity by time interactions. Overall, the torque-velocity curve in the present study shifted downward 13% after BRU with no exercise countermeasure. These results and knee extensor data from previous studies suggest multiple velocity testing is not necessary to characterize strength loss after a period of musculoskeletal unloading.
The impact of bed rest on plantar flexor eccentric strength was previously unknown. We found substantial eccentric strength losses at both slow (0.52 rad·s-1) and fast (2.97 rad·s-1) velocities and decrements in eccentric average power across the velocity spectrum. Our resistance exercise protocol completely ameliorated eccentric strength and power deficits. In a recent NASA roundtable on countermeasure development, it was recommended that “the optimal combination of isometric, eccentric, and concentric contractions that will prevent or attenuate muscle atrophy in weightless environments” be determined (2). As a first step in defining an effective countermeasure our data indicate that, at least for the plantar flexor muscle group, an eccentric:concentric work ratio equal to one is sufficient for maintaining eccentric performance during unloading.
Concentric peak power has been reported to occur at 3.07 rad·s-1(21). Because our fastest test velocity was 2.97 rad·s-1, peak power was not achieved. Velocity-specific concentric power, however, was markedly reduced but only at slow contractile velocities in which power output is relatively low. At faster velocities approaching concentric peak power, velocity-specific power was unaltered (although this may have been in part a result of the greater variability in power seen at faster velocities). REX maintained velocity-specific power and angle-specific torque at all test velocities, indicating our training paradigm offered considerable performance benefits even for velocities much different from the training velocity (approximately 1.05 rad·s-1).
Loss of strength in only the neutral and stretched positions by torque-position analysis in NOE suggests the plantar flexors are most susceptible to strength deficits near in vivo optimal muscle length at which torque capacity is high. At shortened muscle lengths, torque production is minimal and does not appear affected by unloading. The concentric and eccentric torque-position curves were unaltered in REX. Requiring that REX subjects operate through a full range of motion during exercise was probably an important component of our training protocol design.
Changes in contractile strength result from both neurogenic and myogenic factors (28). Reductions in both neural activation(maximum EMG) and muscle size have been found after 6 wk of knee extensor unloading (9,13). We (4) and others (7) have previously reported, however, that knee extensor strength loss after shorter durations of unloading (10-14 d) is not associated with reduced neural activation. In our previous work, myofiber atrophy (17%) accounted for the isometric strength loss (15%)(4). In the present study we did not find any significant reduction in maximum EMG during plantar flexion in either group, suggesting the loss of strength in NOE was primarily due to muscle atrophy.
We and others have reported that strength loss after unloading is preferential to leg extensor muscle groups while strength of the antagonistic flexors changes very little (4,14,17). Lack of change in dorsiflexor MVC in the present study supports these findings. Interestingly, however, maximal neural activation of the tibialis anterior during dorsiflexion was reduced in REX. We previously reported a similar phenomenon for the knee flexors after knee extension-training was performed during bed rest (4). It is well accepted that training benefits are highly specific to the muscle group trained. In ambulatory studies, one neural mechanism for enhanced strength performance after short-term resistance training is inhibition of antagonists(11). Perhaps because the plantar flexors were strenuously exercised and the dorsiflexors were less active throughout bed rest, there may have been some form of inhibition when the dorsiflexors were called upon to contract maximally.
To summarize, in those subjects who did not exercise during bed rest, plantar flexor performance deconditioning was revealed across all modes of contraction tested including 1RM, isometric, isokinetic concentric, and isokinetic eccentric actions. Because no change in maximal EMG was found, it is suggested that loss of performance was caused by muscle atrophy. A 10-min paradigm of five sets of high-intensity (8RM) concentric/eccentric muscle actions performed every other day was very effective in preventing plantar flexor deconditioning during bed rest and the efficacy of training was seen in all contractile modes and across a velocity spectrum. The practical benefits of resistance training found in this study should prove useful in the design of exercise programs for astronauts in microgravity or patients confined to bed rest.
The authors thank Dr. Steven Lieberman and the GCRC nursing staff for outstanding patient care.
;)
Figure 1-Torque-velocity relationship. A: No exercise group. B: Resistance exercise group. *Different from pre within group,: P < 0.05. †Group by time interaction, P < 0.05. ‡Main effect of time, P < 0.05. §Main effect of group, P < 0.05. Values are mean ± SE.
Figure 2-Torque-position relationship. -□- Prebed rest; -▪- Postbed rest; A, Concentric curve for REX; B, Eccentric curve for REX; C, Concentric curve for NOE; D, Eccentric curve for NOE;: df , dorsiflexed region; PF, plantar flexed region.*Region of curve is different from pre within group, P < 0.05. †Group by time interaction, P < 0.05. ‡Main effect of time, P < 0.05.§Main effect of group, P < 0.05. Values are mean± SE.
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