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Research Reports |
RL Gajdosik, PhD, PT, is Professor, Department of Physical Therapy, School of Pharmacy and Allied Health Sciences, The University of Montana, 026 McGill Hall, Missoula, MT 59812 (USA) (rgajdos{at}selway.umt.edu). Address all correspondence to Dr Gajdosik
DW Vander Linden, PhD, PT, is Associate Professor, Physical Therapy Department, Eastern Washington University, Cheney, Wash
AK Williams, PhD, PT, is Professor and Chair, Department of Physical Therapy, School of Pharmacy and Allied Health Sciences, The University of Montana
Submitted May 20, 1998;
Accepted June 9, 1999
| Abstract |
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Key Words: Aged Muscles Passive elastic stiffness Women
| Introduction |
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PRT) to the change in the angle (
A), or
PRT/
A,3,5 may be associated with decreased maximal passive calf MTU length, but this possibility has not been studied. Because therapeutic stretching of the calf muscles is often used to ameliorate deficiencies in ROM, we believe the influence of age on length and PES characteristics of the calf MTU should be studied. Researchers have examined the influence of aging on the PRT2,58 and on the PES5 of passive ankle dorsiflexion within a pre-established dorsiflexion ROM that all subjects could achieve. Chesworth and Vandervoort5 stretched the ankle passively from 10 degrees of plantar flexion to 10 degrees of dorsiflexion and reported no differences in the PRT or the PES among younger (aged 2140 years), middle-aged (aged 4160 years), and older (aged 6180 years) women at 0, 5, and 10 degrees of ankle dorsiflexion. Vandervoort et al2 examined stretching the ankle from 10 degrees of plantar flexion to maximal passive dorsiflexion and found an increase in the PRT at 10 degrees of dorsiflexion for women among increasing age groups (aged 5560, 6165, 7175, 7680, and 8185 years). Neither the maximal PRT nor the PES was reported for the range of passive stretch beyond 10 degrees of dorsiflexion. The authors stated that they limited the stretch ROM to 10 degrees of dorsiflexion because this ROM was within the limits for even the oldest age groups they studied.2 Porter et al6,7 also studied stretching the ankle from 10 degrees of plantar flexion to 10 degrees of dorsiflexion and also reported greater PRT for older women than for younger women at 10 degrees of dorsiflexion. The PRT2,57 and the PES5 reported in these studies were within a dorsiflexion stretch ROM between 10 degrees of plantar flexion and 10 degrees of dorsiflexion for all age groups.
In a study by Winegard et al,8 the ankle was stretched from 20 degrees of plantar flexion to 20 degrees of dorsiflexion, and a curvilinear increase was demonstrated for the PRT at greater dorsiflexion angles for both younger (aged 2030 years) and older (aged 6080 years) men and women. In this study,8 the calf MTU was stretched with the knee flexed to 90 degrees, which decreased the influence of the gastrocnemius MTU on the PRT.9,10 As with the other reports,2,57 this study compared the PRT within a ROM that was common to the subjects in all groups. In all of the studies,2,58 the passive stretch ROM was limited to a dorsiflexion angle common to all subjects, and the calf was probably stretched through an early to middle range of the maximum available length. Thus, the possible influence of the terminal range of extensibility for calf MTU length that would be present in many subjects was not accounted for.
The PRT and the PES of ankle dorsiflexion are influenced by many structures, including the ankle joint capsule and associated ligaments, the calf MTU and associated connective tissues, the superficial fascia, and the skin. The PRT has been shown to increase as the ankle is passively dorsiflexed beyond 10 degrees of dorsiflexion. This increase is primarily explained by the increase in the length of the calf MTU3,4,8 and is especially true with the knee held in extension to include stretching the gastrocnemius muscle.9,10 Because maximal passive dorsiflexion ROM is known to decline with aging, stretching the ankle to the maximal passive dorsiflexion angle available for each subject would also stretch the calf MTU maximally for each subject. Age-related changes in the maximal passive dorsiflexion angle and in the maximal PRT at this angle could be different from the changes measured within the early to middle range of the dorsiflexion stretch.
In a preliminary study,4 we passively stretched the calf MTU maximally with the knee in full extension. We defined the maximal stretch of the calf MTU as the subjects' perceived tolerance to the maximal dorsiflexion stretch or marked electromyographic (EMG) activity at the very end of the stretch, or both. The maximal passive dorsiflexion angle and the angular change from an initial dorsiflexion angle to the maximal dorsiflexion angle (defined as the calf MTU length extensibility) were both decreased for older women (aged 6081 years) compared with younger women (aged 2645 years). The maximal PRT at the maximal passive dorsiflexion angle was less for the older women than for the younger women, but this finding was not statistically significant,4 perhaps because of the small sample size.
The first author (RLG) used similar testing methods with men and showed that the maximal passive dorsiflexion ROM, the maximal PRT, and the average PES of the calf MTU within the last 10 degrees of their maximal available stretch ROM decreased with increasing age groups among younger (aged 2239 years), middle-aged (aged 4157 years), and older (aged 6379 years) men.3 The results of our studies3,4 in which the calf MTU was stretched to the subjects' maximal available dorsiflexion ROM supported the proposal that decreased dorsiflexion ROM may be associated with decreased maximal PRT and decreased PES. Studies have indicated that aging brings about a loss of motor units,1116 a decrease in the number15,17,18 and size15,1721 of both slow-twitch (type I) and fast-twitch (type II) muscle fibers, and the possibility of selective atrophy of type II fibers.1719,21,22 The reduction in the number of motor units and muscle fiber atrophy partially account for the decreased muscle mass and the force deficits reported in the muscles of older people.1416,19,21 In light of the decreased muscle mass and the decreased force associated with aging, the possibility that decreased maximal PRT and PES also would be associated with aging seems plausible. Some muscle in older people may be replaced by increased fat and connective tissue,15,2325 but the relative contributions of increased fat compared with increased collagenous connective tissue have not been related to the changes in the PRT and PES of muscles for older people. Changes in the relative amounts of fat and connective tissue could alter the PRT and PES characteristics of the calf MTU.
The argument that aging may bring about decreased maximal dorsiflexion ROM, decreased maximal PRT, and decreased PES appears to differ with the results of the studies where the calf MTU was stretched through a ROM common to all subjects.2,57 The results of our preliminary studies3,4 led us to design the present study with a larger sample of subjects in order to conduct a more comprehensive investigation. The purpose of this study, therefore, was to examine the influence of age on length and PES characteristics of the calf MTU of active women without known pathology related to the MTU of the calf by passively stretching the ankle through the maximal available ROM that each subject could tolerate. We hoped that the results would contribute to a more complete understanding of the influence of age on length and PES characteristics of the calf MTU of women.
| Method |
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=3.46, SD=0.51; middle-aged women:
=3.79, SD=0.42; older women:
=3.58, SD=0.50), with no differences among the groups (Kruskal-Wallis test=5.71, P=.058). Their mean physical activity levels were rated as fairly active to very active (younger women:
=2.29, SD=0.69; middle-aged women:
=2.63, SD=0.71; older women:
=2.61, SD=0.61), and this rating was also not different among the groups (Kruskal-Wallis test=2.98, P=.225).
Instrumentation
A Kin-Com isokinetic dynamometer (Kinetic Communicator II 500H, software version 4.03)* was used for all passive tests. Data were collected at a sampling rate of 100 Hz. The Kin-Com ankle-foot apparatus was used to stretch the calf MTU by moving the ankle passively into dorsiflexion at 5°·s1. The slow stretch speed of 5°·s1 was used in an attempt to ensure that the stretch did not elicit stretch-induced reflexive muscle activity and because more rapid speeds of passive stretch have been shown to cause increased PRT in the absence of reflexive muscle activity.3,27 We did not check whether the movement of the Kin-Com was as we had set it, but rather we depended on the manufacturer's assurance that the Kin-Com could perform as specified. The PRT was adjusted for the effects of gravity of the apparatus. Surface EMG (GCS 67
) with on-site preamplification was used to monitor the activity of the medial head of the gastrocnemius, soleus, and tibialis anterior muscles to ensure that the stretches were passive during the tests.
The bandwidth of the frequency response was 40 Hz to 4 kHz. The common mode rejection ratio was 87 dB at 60 Hz, and the input impedance was greater than 25 M
at direct current. The raw EMG signals were relayed to an amplifier (x 5,000) and filtering system, and the analog signals were converted to digital signals at a sampling rate of 500 Hz and monitored during the tests. The EMG tracings were monitored during the tests in an effort to ensure that calf muscle activity was less than 0.05 mV above baseline during the passive stretch trials.
Procedure
All subjects assumed a supine position on an examination table, and the most prominent aspects of the right fibular head and the medial and lateral malleoli were palpated and marked with a felt-tipped pen by the first author. A line was drawn between the fibular head and lateral malleolus to represent the longitudinal axis of the leg. The axis of the ankle was estimated using a procedure described previously.28
The subjects then completed a regimen of supervised static calf MTU stretching to help ensure that a maximal passive dorsiflexion would be achieved during the passive stretching tests. The left foot was placed on the floor in front of the body with the knee slightly bent, and the subjects were instructed to keep the right knee straight and the heel on the floor. They then stretched the right calf MTU by moving the right ankle into dorsiflexion until they felt a maximal stretch, as tolerated. They completed 10 repetitions of 10 seconds of static stretching during each repetition.
After stretching, the surface EMG electrodes were attached over the muscle bellies of the medial head of the gastrocnemius muscle, the soleus muscle, and the tibialis anterior muscle. The subjects then assumed a supine, relaxed position on the Kin-Com table with the right knee fully extended. Using a level, the longitudinal axis of the leg was aligned parallel with the horizontal plane, the ankle and foot were positioned in the apparatus, and the ankle was aligned with the axis of the Kin-Com armature. The foot was secured with a bandage wrap, and stabilization straps were placed across the right knee, pelvis, and chest. Using oscilloscope tracings of the EMG signals from the muscles, the subjects were taught to recognize EMG activity and EMG silence of the muscles. They were then encouraged to maintain flat EMG tracings during the test session, which was conducted in a quiet room with the lights dimmed.
The maximal passive dorsiflexion angle was determined by manually moving the ankle in the apparatus slowly into dorsiflexion for several trials without EMG activity in the calf muscles. The end point of dorsiflexion ROM was defined by either a marked presence of EMG activity in the calf muscles or the part of the stretch just prior to the point that caused pain or discomfort. Most subjects learned to relax their muscles, but 7 subjects were excluded because they could not adequately relax their muscles so that the EMG activity was less than 0.05 mV above baseline. Because the subjects received relaxation training and numerous manual calf MTU passive stretches before the examiner established the end point of the dorsiflexion stretch, the end point was defined as being just prior to discomfort in the majority of the subjects. Based on ethical considerations and approval of the testing protocol by The University of Montana Institutional Review Board for the Use of Human Subjects in Research, the subjects' perceived tolerance to the maximal passive stretch was the primary criterion used for determining the maximal dorsiflexion angle, which we believed characterized the maximal length of the calf MTU. Because the maximal dorsiflexion angle was determined based on psychophysiological phenomena, we acknowledge that this end point of dorsiflexion ROM was not necessarily a true mechanical end point of maximal calf MTU length.
After the maximal dorsiflexion angle was found, the ankle-foot apparatus was moved from this angle through 60 degrees into plantar flexion. The ankle was then stretched passively by the Kin-Com from this relaxed plantar-flexion position through the 60-degree ROM to the predefined maximal dorsiflexion angle. Ninety degrees was defined as neutral (0°), degrees of dorsiflexion were positive, and degrees of plantar flexion were negative. Three trials were performed at the predetermined speed of 5°·s1. Because one older subject expressed discomfort with her ankle positioned in plantar flexion, her ankle was stretched through a 55-degree ROM into dorsiflexion. After each trial, the foot was returned to the starting plantar-flexion angle at 5°·s1. Because calf muscle EMG activity (shortening response) was observed in some subjects when the calf MTU was passively shortened into plantar flexion, the examiner (RLG) applied Achilles tendon pressure by squeezing the medial and lateral aspects of the tendon,29 and time was allotted between trials in an attempt to ensure that the muscles were without EMG activity at the beginning of all stretching trials.
Data Reduction
The maximal dorsiflexion angle was defined as 1 degree less than the maximal passive dorsiflexion angle that was determined manually and used during the stretching trials. Subtracting 1 degree of dorsiflexion accounted for the small deceleration artifact and an observed loss of Kin-Com angle data at the end of the ROM that has been documented previously.30 The maximal PRT was measured at this adjusted maximal passive dorsiflexion angle. We then calculated 10% of the maximal PRT and used this value to define an initial passive dorsiflexion angle. The difference between this initial dorsiflexion angle and the maximal dorsiflexion angle was called the angular change, which was the full stretch ROM and represented the calf MTU length extensibility.4 A list of the variables used in this study and their definitions is presented in Table 2.
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PRT) was differentiated at 0.5-degree intervals (
A) within the full stretch ROM using a customized software program (written by Dr Peter McNair, Auckland Institute of Technology, Auckland, New Zealand). The PES (
PRT/
A) at each differentiated interval was then averaged for the full, defined stretch ROM (angular change) and for the first half and the last half of this full, defined angular change of the passive curves. A third-order polynomial function was used because a preliminary study of the data indicated that the coefficient of determination of the fitted curve was near 1 (r2=.998), and higher-order polynomial functions (fourth order to seventh order) did not improve the predicted average PES. The following variables were averaged among trials: the maximal PRT, thepassive angular change, and the predicted average PES for the full, defined stretch ROM and for the first half and the last half of this stretch ROM. The reliability and the precision of the method used to determine the maximal passive dorsiflexion angle and the maximal PRT were examined in a test-retest study with a separate group of subjects (n=10). The intraclass correlation coefficient (ICC[2,3]) and the standard error of measurement (SEM) for measuring the maximal dorsiflexion angle were .91 and ±1.2 degrees, respectively. The ICC and SEM for measuring the maximal PRT were .90 and ±3.9 N·m, respectively. The ICCs and the SEMs indicated excellent reliability and precision for these measurements.
During the actual study, we also documented the coefficient of variation (CV) for the maximal PRT and for the mean PRT through the full stretch ROM among the trials for a random sample of 15 subjects in each age group. The mean CVs for the maximal PRT were 2.00% for younger women, 2.93% for middle-aged women, and 3.00% for older women. The mean CVs within the full stretch ROM were 1.73% for younger women, 2.07% for middle-aged women, and 2.67% for older women. The small CVs for each age group indicated to us that there was minimal variability among the 3 test trials, thus demonstrating good consistency within the test session. In addition, we also addressed the potential for entering systematic errors into the results over the course of the study by calibrating the Kin-Com according to the manufacturer's guidelines before each day of testing and by randomly testing the women from among the 3 age groups over the course of the study.
Data Analysis
A multivariate analysis of variance (MANOVA, Pillai Trace) was used to examine the effects of age groups on the following variables: (1) maximal passive dorsiflexion angle, (2) maximal PRT, (3) angular change, (4) average PES for the full, defined stretch ROM, (5) average PES for the first half of this stretch ROM, and (6) average PES for the last half of this stretch ROM. The MANOVA was followed by a separate one-way ANOVA for each dependent variable, and significant ANOVAs were followed by Tukey post hoc analyses to examine group differences.
The Pearson product-moment correlation coefficient was used to examine the strength of the relationship of age to each variable. The level of significance was set at P
.05.
| Results |
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=15.39°, SD=5.78°) compared with the younger women (
=25.83°, SD=5.5°) and the middle-aged women (
=22.75°, SD=4.38°) (P<.001). The passive angular change for the older women (
=25.41°, SD=9.72°) was less than the passive angular change for the younger women (
=37.75°, SD=5.51°) and the middle-aged women (
=32.96°, SD=7.83°) (P
.003). The maximal PRT for the older women (
=12.61 N·m, SD=5.69) also was less than the maximal PRT for the younger women (
=21.68 N·m, SD=5.33) and the middle-aged women (
=17.95 N·m, SD=5.43) (P
.002).
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=0.59, SD=0.20) than for the younger women (
=0.74, SD=0.19) within the last half of their respective dorsiflexion stretch ROMs (P=.019). The average PES between the younger and middle-aged women and between the middle-aged and older women did not differ within the last half of the full, defined stretch ROM.
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| Discussion |
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The decreased maximal passive dorsiflexion angle for the older women supports the results of previous studies showing that the calf MTU is shortened in older people.14 This decreased length of the calf MTU for the older women truncated the maximal passive dorsiflexion angle of the passive curves to the left, yet the initial passive dorsiflexion angle (where the PRT was 10% of the maximal PRT) was similar among age groups. The lack of differences among groups for the initial passive dorsiflexion angle agrees with our previously published report using this testing method.4 The calf MTU shortening for the older women could have resulted from changes similar to those reported for animal muscles. Animal muscles immobilized in the shortened position showed decreased muscle length because of a reduction in the number of sarcomeres.3539 Although the calf MTUs for the older women in the study were not immobilized, the shortened calf MTUs for the older women could have resulted from the subjects not performing physical activities that required greater calf MTU lengthening or may indicate that they did not routinely stretch the calf MTUs maximally. We acknowledge that different results may be found for very sedentary women or for women who engage in very intense physical activities. The women in the age groups that we studied rated their activity levels as fairly active to very active. Differences in the physical activities for the women that we studied, therefore, are not a likely explanation for the decreased maximal passive dorsiflexion angles we observed.
Studies that have examined skeletal muscle adaptations in animal models as a result of immobilization in the shortened position have shown a distinct relationship between muscle atrophy from disuse and decreased muscle length.35,40 Accordingly, it is plausible that calf MTU shortening during aging can occur concomitantly with the loss of motor units1116 and muscle mass and force.1416,19,21 The older women in our study also had decreased maximal concentric isokinetic plantar-flexion torque, as we reported elsewhere.31 The decreased maximal PRT and the decreased PES for the older women could have resulted from the loss of motor units1116 and a decrease in the number15,17,18 and size15,1721 of both type I and type II muscle fibers that decreased the mass of the muscles. The loss of muscle mass, combined with the decreased calf MTU length related to aging, could decrease the calf MTU's ability to withstand a maximal passive stretch to the women's tolerance.
Compared with the younger women, the older women had about 80% of the PES within the last half of their respective full, defined stretch ROMs. Within this last half of the stretch ROM, the older women also had about 68% and 56% of the younger women's change in dorsiflexion ROM and change in PRT, respectively. Because the PES was calculated as
PRT/
A, these comparisons suggested that the loss of PRT probably had a greater relative contribution to the decreased PES than the loss of passive dorsiflexion ROM. The lack of age group differences in the PES within the first half of the stretch ROM was similar to the results of the study by Chesworth and Vandervoort5 in which the ankle was moved from 10 degrees of plantar flexion to 10 degrees of dorsiflexion, an early to middle range of ankle joint dorsiflexion stretch ROM.
Our expanded analysis revealed no difference among groups for the PES at 0, 5, 10, and 15 degrees. The PES at 5 and 10 degrees of dorsiflexion compared favorably with the findings of Chesworth and Vandervoort.5 Our results, however, are not in agreement with those of Porter et al,6,7 who found increased PRT at 10 degrees of dorsiflexion for older women compared with younger women. Porter et al6,7 tested the subjects in the standing position, so different testing methods could partially account for their results. Further study is needed to address this possibility. Our results demonstrated that stretching the calf MTU maximally according to each subject's tolerance provides a different profile of ankle PRT than has been described previously,2,58 although our results also support previously published reports.35
Replacement of the calf muscle tissue with adipose tissue also could have contributed to the decreased average PES for the older women. Previous studies with humans have shown that the lost muscle mass in older people may be replaced by increased adipose and other connective tissues within the muscles.15,2325 Based on the results of studies of the connective tissue arrangement of the perimysium of skeletal muscles,4143 increased amounts of relatively inextensible collagenous connective tissue should bring about greater tension per unit of length change, which should increase the PES of the muscles, particularly in the last half of the stretch ROM. Increased PES was not observed in our study, which suggests that if lost muscle tissue was replaced by fat and connective tissue, the amount of fat and connective tissue was probably insufficient to counteract the lost muscle mass necessary to increase the PES. Furthermore, experimental evidence from rabbit soleus muscles has indicated that connective tissue accumulation that occurs in inactive muscles can be prevented by passive stretch or by active stimulation.44 In this study with rabbit soleus muscles,44 the lack of connective tissue accumulation was demonstrated in muscles that worked over a reduced ROM, even though there was a reduction in the number of sarcomeres similar to when animal muscles were immobilized in the shortened position. A minimal level of physical activity may prevent the accumulation of connective tissue in the aged calf MTU of active women. The PES of very inactive, sedentary women may be different from that of the women we tested. In order to address these possibilities, future studies would need to examine the relative amounts of adipose and collagenous connective tissue of aged human calf MTUs in conjunction with examining their muscle mass, passive length, PRT, and PES characteristics.
Clinical Implications
Our finding that the older women had decreased maximal passive dorsiflexion ROM, together with decreased maximal PRT and decreased PES in the last half of the full, defined stretch ROM, appears to suggest that decreased dorsiflexion ROM, also sometimes referred to as "decreased flexibility," is not associated with increased stiffness. We demonstrated that the older women had less maximal passive dorsiflexion ROM, decreased maximal PRT, and decreased PES within the last half of their available stretch ROM when compared with the younger women. These findings were supported further by the negative association of age with the length and stiffness variables. According to our results, older active women with decreased dorsiflexion ROM would have less resistance to passive stretching at their maximally tolerated dorsiflexion limit compared with younger women. Increased length of the calf MTUs of active women with no known related pathologies, as indicated by increased dorsiflexion ROM, appears to be associated with increased maximal PRT and increased PES. The relationship of calf MTU length, maximal PRT, and PES for inactive, sedentary women or for patients such as those with conditions that cause peripheral neuropathies45 or central nervous system deficits46 may be very different from that of the sample of women we tested.
In active people without pathology that may affect the calf MTU, limited passive dorsiflexion ROM due to shortening of the calf MTU, combined with decreased calf muscle force,47 may limit the ability to respond to anterior postural perturbations and to generate the forces needed to control the center of mass.48,49 These changes may impede normal ambulation and contribute to falls among elderly people. Therapeutic interventions designed to both lengthen and strengthen the calf MTU should enhance calf MTU function or help to prevent age-related declines in calf MTU function. These possibilities are particularly worthy of future study.
| Conclusions |
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| Footnotes |
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The study was approved by The University of Montana Institutional Review Board for the Use of Human Subjects in Research.
This study was supported by grants from the American Association of Retired Persons (AARP) Andrus Foundation, the MJ Murdock Charitable Trust Foundation, and The University of Montana.
* Chattecx Corp, 101 Memorial Dr, PO Box 4287, Chattanooga, TN 37405. ![]()
Therapeutics Unlimited Inc, 2835 Friendship St, Iowa City, IA 52245. ![]()
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