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a School of Rehabilitation Therapy, Physical Therapy Program, Faculty of Health Sciences, Queen's University, Kingston, Ontario, Canada
b School of Physical Therapy, Faculty of Health Science, University of Western Ontario, London, Canada
Anthony A. Vandervoort, School of Physical Therapy, Room 1400, Elborn College, The University of Western Ontario, London ON, Canada N6G 1H1 E-mail: vandervo{at}julian.uwo.ca.
Jay Roberts, PhD
| Abstract |
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PRODUCTION of absolute maximal torque is known to be reduced by aging (1)(2)(3)(4). Less is known regarding the ability to produce explosive torque in a timely fashion, although fast, forceful contractions may be critical to maintain balance and to prevent trips and falls in an older adult. In normal postural control, the time taken to produce a submaximal force may sometimes be as important as the absolute force level itself (5)(6). For example, the age-related loss of high muscle torque levels in the ankle (7)(8)(9) may be restrictive to the fast, forceful muscle contraction responses needed to respond effectively to perturbations of posture. In addition, diminished sensorimotor conduction might produce significant delays of long-loop reflexes in response to challenges to balance (6)(10).
Previous analyses of torque-time, torque-velocity, and length-tension curves for isometric or concentric (CONC) contractions of the ankle dorsiflexor muscle group (8)(9)(11) and of torque-angle isokinetic curves at 30°/s for CONC and eccentric (ECC) dorsiflexor muscle actions (7) indicate that explosive torque production capacity of this muscle group decreases in older people. These findings support the concepts that age-related atrophy effects may be greater on fast-twitch than on slow-twitch fibers, that there is a loss of fast-twitch fibers, or that the maximal rate of voluntary neural activation of the muscles might also be reduced by aging (5)(12). The type II muscle atrophy observed in elderly persons has been associated with a greater decrease in torque at higher isokinetic velocities and with lower maximal peak knee extension velocities (13)(14), but a similar study was not found for the dorsiflexor muscle.
Observations that aging limits the ability to produce fast, forceful muscle contractions at higher velocities of movement prompt the question: Can training these movements over time promote a neural adaptation to improve peak torque and power at faster movement speeds? Evidence suggests that ECC torque is preserved to a greater extent than CONC torque (7)(15)(16) in older persons, leading to the possibility that training with ECC loading is an effective approach for this age group (17). Nevertheless, the effects of aging on ECC dorsiflexor strength over faster velocities have also received insufficient attention to date. Thus, the purposes of this study were to quantify CONC and ECC dorsiflexor muscle strength at various movement speeds and to determine the neuromuscular effects from short-term practice of repeated maximal voluntary contractions using an isokinetic resisted exercise program in older adults.
| Methods |
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Torque Measurement Equipment
Dynamic CONC and ECC action torques were measured on a Kin-Com 500H isokinetic dynamometer with version 3.21 software (Kinetic Communicator, Chattecx, Chattanooga, TN). The Kin-Com ankle unit and universal stabilizer attachments were used with the subject seated in the standard positioning for ankle plantar and dorsiflexor muscle exercise (outlined in the operator's manual). The ankle plantar/dorsiflexion attachment was fitted onto the lever arm with the load cell at a constant 0.21 m distance for all subjects. A preload of 10 N · m, approximately 10% of the subject group's average maximal voluntary torque, was programmed into the protocol to decrease acceleration and deceleration phases in the ankle movement. The dynamometer head was fixed in the lowest height position with the universal stabilizer attachment in place under the leg to be tested.
Subjects performed exercise with their shoes on and wore the same shoes for all training and testing sessions. Extra padding to secure the foot into the ankle unit was thereby minimized, the foot was easily stabilized, and pressure from the strapping was modified to accommodate bunions and hammer toes. Lifting of the heel, especially during a plantar flexion movement, and sliding of the foot in the ankle unit was also diminished with a shod foot.
Subject Positioning
The subjects sat on the Kin-Com seat against a back support with their foot resting in the ankle unit. The seat was adjusted so that the knee was flexed to 90° with the ankle in neutral. The universal stabilizer was adjusted to support the calf or thigh. Stabilizing belts were secured over the lap, thigh or shin (depending on the height of the subject), ankle, and forefoot to prevent extraneous movement. Foam padding was placed between the popliteal fossa and the universal attachment and between the foot and stabilizing belts at the ankle and forefoot to minimize discomfort during contractions. The rotational axis of the dynamometer was positioned to be coaxial with the ankle joint axis of plantar and dorsiflexion (fibular malleolus) during testing (19). The resistance pad was positioned directly under the heads of the metatarsals. During testing, subjects were asked to keep their arms folded across their chest.
Training Procedures
At the beginning of each training session, a warm-up consisted of sets of 6 repetitions (reps) of uninterrupted cycles of CONC dorsiflexion paired with CONC plantar flexion performed at each of 30°, 90°, and 180°/s velocities. These velocities were chosen based on previous literature and the capabilities of older adults. Another 6 reps were performed, as previously described, in reverse order with CONC plantar flexion followed by CONC dorsiflexion. The range of movement for training was individualized for subjects based on their pain-free active ankle joint range of movement and standardized for the remaining training sessions for that subject. The target ankle range of movement for training was 0° to 40° (or as near as possible) for individual subjects. This range of movement was in reference to the position of the ankle unit, with 0° or neutral ankle range of movement defined as the fifth metatarsal perpendicular to the midline of the leg, as measured by a goniometer, and 40° into ankle plantar flexion. The right leg for all subjects was chosen to be the experimental leg for the training program. A pre- and postexercise session were completed using the subjects' left leg as the control.
Two sets of 12 MVCs of the ankle dorsiflexor muscles were performed during each training session, at each of the three velocities30°, 90°, and 180°/s for the right (trained) leg. The specific training protocol involved 6 cyclic (uninterrupted) CONC dorsiflexion/ECC dorsiflexion MVCs and 6 cyclic ECC dorsiflexion/CONC dorsiflexion MVCs. A 2-minute rest was given between the sets of 6 cycles at each velocity, and a 5-minute rest was given between CONC/ECC and ECC/CONC dorsiflexion contraction sequences. Training occurred three times per week over 2 weeks.
The subjects were instructed to "pull" for CONC and ECC dorsiflexion "as hard and as fast as possible," but were not verbally encouraged for maximal output during the contractions. The investigator did, however, coach subjects for effective breathing during the maximal efforts to avoid increased intrathoracic pressures. Assurance from the subjects was sought periodically during rest periods to reinforce that they were performing MVCs at each velocity, throughout their full range of movement.
Isokinetic Peak Torque
The gravity correction factor (correcting for additional torque produced by the foot and leg segment mass) was determined at the beginning of each set of contractions by identifying the subject's leg-foot segment mass at a static position near their end relaxed plantar flexion range of movement. The resultant gravity-corrected torques were used for analysis. To avoid inertial artefacts due to acceleration and deceleration periods of the movement, only torque data during the constant velocity portion of the range of motion were analyzed. The constant velocity periods were provided by filtering data by velocity in a statistical package (SigmaStat, SPSS, Inc, Chicago, IL). Constant velocity was limited to 30° ± 1°/s, 90° ± 1°/s, or 180° ± 1°/s over the entire training range of movement. Only dorsiflexor torque achieved at the 30°, 90°, or 180°/s set velocity was included in the analysis. The force data was transformed to torque using a lever arm length of 0.21 m for all subjects, based on the distance of the load cell from the axis of rotation on the dynamometer head. For each subject, the highest dorsiflexor CONC and ECC peak torques achieved at 30°, 90°, or 180°/s were selected as the peak torques for each training session. Peak torque values for CONC dorsiflexion were taken from contraction sequences when CONC preceded ECC dorsiflexion, and ECC peak torque values were collected from contraction sequences when ECC preceded CONC dorsiflexion.
In addition to the comparison of peak torques, the torque-angle relationships were examined for CONC and ECC dorsiflexion actions on pretest versus post-test. Velocity-filtered torque for each set of 6 CONC or 6 ECC dorsiflexion contractions was plotted against ankle range of movement at pretest and post-test to produce the strength curves for each subject. The strength curves for all subjects (N = 28) were plotted on the same graph to compile a representative strength curve for the subject group. A CONC and ECC dorsiflexion strength curve was made for each movement speed.
The angle at which CONC dorsiflexor peak torque occurred was collected from the velocity-filtered force data (converted to torque) and used to calculate the rate of torque development for each of the training velocities for each subject. From the angle of peak torque, the time to reach peak torque could be calculated based on the angular velocity (30°, 90°, or 180°/s). The ankle range of motion to the angle of peak torque was determined by subtracting the angle of peak torque from the start position of the contraction (measured in degrees). Time to reach peak torque angle was determined by dividing the ankle range of movement for peak torque (°) by the velocity of movement (°/s). The average rate of torque development [i.e., peak torque (N · m)/time (s)] was then calculated using the peak torque and time to reach this angle, as previously published (7).
Electromyography
Surface electromyographic (EMG) recordings were made from one agonist (tibialis anterior) and a representative antagonist (soleus) muscle. Agonist dorsiflexor (tibialis anterior) and antagonist plantar flexor (soleus) EMG was collected using 10 mm-diameter Beckman silver-silver chloride surface electrodes (Sensormedics Corp, Anaheim, CA) with a 16-channel, fiber-optic, biological amplifier (total gain 2000x, low-pass filter 1000 Hz, high-pass filter 10 Hz, common mode rejection ratio >70 dB at 100 Hz, sampling frequency 2500 Hz), custom-made system (Paul Guy Circuits Design, Waterloo, ON, Canada). EMG data were full-wave rectified and low-pass filtered at 3 Hz to produce a linear envelope prior to analog/digital (A/D) conversion and storage by an IBM 386 compatible computer. A custom-designed software program (MEMG; C.Y. Yim Custom Software, Inc, Toronto, ON, Canada) sampled the digital EMG signal at 200 Hz/channel before EMG integration was completed.
Skin preparation, electrode placement, and recording procedures were standardized over the study period. Alcohol pads were used to clean the skin, followed by abrasion with a terry cloth towel and conducting gel until an erythema was produced. Two Beckman silver-silver chloride surface electrodes (Sensormedics Corp, Anaheim, CA), with an 8-mm diameter well, were positioned and fixed with collars overlapping and straddling the center of the muscle bulk of the tibialis anterior, approximately 5 cm superior to the muscle-tendon junction. The surface electrodes were placed during a maximal voluntary toe-raise contraction. Plantar flexor-recording electrodes were positioned during a heel raise over the soleus muscle, just lateral to the midline of the leg, and approximately 5 cm inferior to the bulk of the gastrocnemius. The ground electrode for the dorsiflexor channel was fixed over the head of the fibula. A ground electrode fixed over the lateral malleolus completed the plantar flexor channel circuit. The electrode positions were measured to minimize variability in electrode placement when retesting.
Mean EMG was calculated as the integral from the beginning to end of the CONC or ECC phase of dorsiflexor muscle contraction for the 3 most consistent, smoothest repetitions of the set (20). These 3 integrals were then averaged to produce the final mean EMG value for the training day measured in millivolt · seconds (mV · s). The potentiometer reading of lever arm angle (joint position) from the Kin-Com was processed concurrently with the linear envelope EMG data through the A/D board so that ankle joint angle position would be in "real time" beside the EMG data. By this connection, EMG specific to the CONC or ECC muscle action were analyzed.
Statistical Methods
The torque and the agonist tibialis anterior and antagonist soleus EMG data for the right (trained) leg were analyzed with a three-factor (time, velocity, contraction type) repeated measures analysis of variance (ANOVA; Unixstat 5.2). Post hoc analysis was performed for significant interactions using Tukey's test, which is a conservative method (21). The p < .05 level was used to establish statistical significance for post hoc comparisons. Critical values of the studentized range statistic, q, for Tukey's tests were determined from the Tukey table based on the total number of means in the comparison (r) and the dfe (21). Also, paired t tests on the right (trained) leg data were performed to compare rate of torque development over time at each velocity. The p < .05 level was used to establish statistical significance. Left leg (control) data for torque were analyzed with a three-factor (time, velocity, contraction type) repeated measures ANOVA.
| Results |
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| Discussion |
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Strength curves are important indicators of muscular capability to exert torque through range (26). The strength curves at 30° and 90°/s, for both CONC and ECC dorsiflexion, were shifted upward after the 2-week training period, representing increased torque production and some leftward displacement in the angle at which peak torque occurs at post-test. This leftward shift in peak torque angle, for CONC dorsiflexion more than ECC dorsiflexion, indicates the increased rate of torque development produced with training. Little change was found between pretest and post-test strength curves at 180°/s. These smallest changes at the highest movement velocity reflect the difficulty subjects had producing torque at this highest training/testing velocity and suggest that a greater amount of training is required to increase torque production in older adults at high movement velocities. Alternately, reduced torque production at high velocity suggests some loss of type II fibers and a reduced ability to perform fast contractions. However, it was encouraging to observe significant improvements in the rate of peak torque development for CONC dorsiflexion at 30°, 90°, and 180°/s. This increase in rate of peak torque development after several training sessions would appear to reflect an important improvement in the capacity of the nervous system to drive the muscle towards more rapid torque production.
This study presents an initial representation of CONC and ECC dorsiflexion torque-angle curves for older adults at velocities greater than 30°/s. The steep decline in torque production at increasing speeds during CONC dorsiflexion movements (Fig. 1) demonstrates a rapid loss of capacity for fast, forceful shortening contractions at the ankle joint in older adults. The results definitely illustrate the compromised rate of torque development with increasing movement velocity (Table 2 ) and appear to be near the limits for torque production at 180°/s for these older adults. Training effects from a short-term intensive training protocol suggest that neural factors can be retrained to improve peak torque production. However, improved torque at faster movement speeds requires a longer program or greater training volume to effect significant changes. In addition, ECC strength appears to be preserved with aging to a greater extent across movement velocities than CONC muscle work. The preserved level of ECC dorsiflexion strength in this group of older adults was also somewhat resistant to the short-term training program as greater effects were seen in CONC dorsiflexion torque-angle curves at 30° and 90°/s movement velocity.
Training-induced neural adaptations in this study were measured indirectly by analyzing changes that took place in EMG activity of the trained agonist dorsiflexor muscles during MVCs at various movement speeds. Increased agonist EMG represents an increase in net excitation of the motoneurons secondary to an increased excitatory input from a greater number of motoneurons that are active and/or an increased firing rate of already active motoneurons. Increased agonist activity, as measured by EMG, can result from increased excitatory input or be increased as a result of reduced inhibitory input, or both (22)(27). Using the surface EMG method, it was not possible to determine whether the mechanism for increased EMG was increased firing rate or increased number of active motoneurons.
One theory for increasing firing rate in the agonist muscle and thereby increasing force production is the reflex inhibition mechanism (27). Reflex inhibition of the antagonist muscles during agonist activity is thought to reduce the opposition to agonist contraction, thereby increasing force production. However, the level of coactivation of the opposing plantar flexor muscle group remained unchanged over the training period and suggests that, in this group, a reduced level of co-contraction facilitating increased agonist torque production did not occur. In addition, dorsiflexion peak torque occurred in the lengthened position of the muscle, at which time the plantar flexor muscle group was quite shortened and less capable of producing antagonist force.
Another mechanism for the increase in muscle activation may result in part from possible adaptations in the recruitment pattern of the activated motor units (6)(22). Previous work by Moritani and colleagues (28) found that after 2 weeks of biceps strength training at 30% MVC, EMG was significantly increased, and the mechanism proposed was synchronization of motor unit firing. Mean power frequency analysis reflected a shift toward lower frequency bands due possibly to better summation or synchronization of the underlying action potentials (29). Increased coordination of neural stimulation at the onset of a muscle contraction, to counteract the slower-contracting muscle of older adults (9)(25), could be advantageous for increased force production.
Learning to recruit the larger fast-twitch motor units for these fast velocity MVCs has been hypothesized as an important advantage for rapid ballistic movements (22). There are still some fast-twitch fibers remaining in the muscle of older adults (12), and occasional high maximal motor unit firing rates, as found in young muscle, have been measured in aged muscles using the intramuscular recording techniques (30)(31)(32). Thus, in the present study, one of the mechanisms for the increased torque could be due to learning to prime the neuromuscular system to more readily recruit additional motor units and/or discharge the already active motor units with higher frequency, perhaps with some neural pathways that also involve the segmental reflex loops (22)(29).
In summary, rapid increases were observed in EMG, CONC and ECC peak torque, and the rate of torque development of the ankle dorsiflexor muscles across three velocities in older adults who performed several sessions of isokinetic strength training. These improvements in the short time frame investigated indicate that considerable training-induced adaptation takes place in the neuromuscular control system. This study concluded that training high velocity movements is feasible for older persons, and further study is warranted on the value of this approach, including dynamic/isotonic movements, for enhancing functional mobility and prevention of falls.
| Acknowledgments |
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Received May 24, 1999
Accepted February 19, 2000
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