Influence of Age on Length and Passive Elastic Stiffness Characteristics of the Calf Muscle-Tendon Unit of Women.

Key Words: Aged, Muscles, Passive elastic stiffness, Women.

Decreased length of the calf muscle-tendon unit (MTU), defined as the decrease in dorsiflexion range of motion (ROM) with the knee extended, is associated with normal aging in both men[1-3] and women.[1,2,4] The common use of the terms "decreased flexibility" or "increased stiffness" in association with the decrease in maximal passive dorsiflexion ROM implies that shortened calf MTUs may become stiffer with aging, even in active adults without related pathologies. We believe that changes in maximal passive resistive torque (PRT) to passive dorsiflexion stretch and changes in passive elastic stiffness (PES), defined as the ratio of the change in the PRT ([Delta]PRT) to the change in the angle ([Delta]A), or [Delta]PRT/[Delta]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 PRT[2,5-8] and on the PES[5] of passive ankle dorsiflexion within a pre-established dorsiflexion ROM that all subjects could achieve. Chesworth and Vandervoort[5] 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 21-40 years), middle-aged (aged 41-60 years), and older (aged 61-80 years) women at 0, 5, and 10 degrees of ankle dorsiflexion. Vandervoort et al[2] 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 55-60, 61-65, 71-75, 76-80, and 81--85 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? Porter et al[6,7] 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 PRT[2,5-7] and the PES[5] 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 20-30 years) and older (aged 60-80 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,[2,5-7] this study compared the PRT within a ROM that was common to the subjects in all groups. In all of the studies,[2,5-8] 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 MTU[3,4,8] 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 60-81 years) compared with younger women (aged 26-45 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 22-39 years), middle-aged (aged 41-57 years), and older (aged 63-79 years) men.[3] The results of our studies[3,4] 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,[11-16] a decrease in the number[15,17,18] and size[15,17-21] of both slow-twitch (type I) and fast-twitch (type II) muscle fibers, and the possibility of selective atrophy of type II fibers.[17-19,21,22] 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.[14-16,19,21] 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,[15,23-25] 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.[2,5-7] The results of our preliminary studies[3,4] 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

Subjects

Eighty-one women (aged 20-84 years) participated with informed consent. The women were assigned to 1 of 3 groups based on their age: (1) younger women (aged 20-39 years, n=24), (2) middle-aged women (aged 40-59 years, n=24), and (3) older women (aged 60-84 years, n=33). Descriptive statistics for the subjects' age, height, mass, and body mass index (BMI=mass [kg] /height [[m].sup.2]) are presented in Table 1. A one-way analysis of variance (ANOVA) indicated that the BMIs did not differ among groups (F=2.16; df=2,78; P=.12).

Table 1.

Descriptive Statistics for Age, Height, Mass, and Body Mass Index (BMI) for Younger Women (n=24), Middle-aged Women (n=24), and Older Women (n=33)

                       [bar]X    SD        Range

Age (yr)
  Younger women         29.7     6.2       20-39
  Middle-aged women     50.2     6.1       40-59
  Older women           72.9     7.3       60-84
Height (cm)
  Younger women        165.67    4.65   159.00-178.00
  Middle-aged women    162.75    5.66   154.00-173.00
  Older women          158.76    5.23   150.00-175.00
Mass (kg)
  Younger women         62.19    7.92    48.20-77.30
  Middle-aged women     61.99   10.16    42.70-86.40
  Older women           60.80    7.05    49.10-79.60
BMI
  Younger women         22.63    2.48    18.83-27.07
  Middle-aged women     23.32    3.09    16.89-28.87
  Older women           24.13    2.58    20.29-30.33

(a) BMI=mass (kg)/height [(m).sup.2].

All women were without a history of orthopedic or neurological disorders, and they were considered non-sedentary and active for their particular age groups. Although physical activities varied both within and among the groups, all subjects reported participating in routine moderate to strenuous physical activities such as gardening, walking, hiking, running, dancing, or aerobics. Self-report of physical activity was used because it was economical and efficient.[26] The subjects self-assessed their current general health status as excellent, good, fair, or poor. They also rated their physical activity level as extremely active, very active, fairly active, or minimally active. Rankings of 1 to 4 were given to the self-ratings, with 4 being excellent general health or extremely active. All of the women rated their current general health as good to excellent (younger women: X=3.46, SD=0.51; middle-aged women: X=3.79, SD=0.42; older women: X=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: X=2.29, SD=0.69; middle-aged women: X=2.63, SD=0.71; older women: X=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-Cum 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-Cum ankle-foot apparatus was used to stretch the calf MTU by moving the ankle passively into dorsiflexion at 5 [degrees] [multiplied by] [s.sup.-1]. The slow stretch speed of 5 [degrees] [multiplied by] [s.sup.-1] 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-Cum was as we had set it, but rather we depended on the manufacturer's assurance that the Kin-Cum could perform as specified. The PRT was adjusted for the effects of gravity of the apparatus. Surface EMG (GCS 67([dagger])) 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[Omega] 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-Cum 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-Cum 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]), degrees of dorsiflexion were positive, and degrees of plantar flexion were negative. Three trials were performed at the predetermined speed of 5 [degrees] [multiplied by] [s.sup.-1]. 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 [degrees] [multiplied by] [s.sup.-1]. 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.

Table 2.

List of the Terms and Their Abbreviations and Definitions

Terms and Abbreviations            Definition

Maximal dorsiflexion angle         Angle at which subject could not
                                    tolerate further stretch into
                                    dorsiflexion or angle at which
                                    electromyographic activity from
                                    the calf muscles was observed.
                                    Angular measurement that defined
                                    the end of the passive curve and
                                    represented the maximal passive
                                    calf muscle-tendon unit (MTU)
                                    length.
Maximal passive resistive torque   Resistance to passive
 (maximal PRT)                      dorsiflexion stretch measured at
                                    the maximal dorsiflexion angle.
Initial dorsiflexion angle         Ankle angle where the passive
                                    resistive torque was 10% of the
                                    maximal PRT. This angle defined
                                    the beginning of the passive
                                    curve.
Angular change                     Angular distance between the
 (ANG-CH)                           initial dorsiflexion angle and
                                    the maximal dorsiflexion angle.
                                    This angular distance defined
                                    the full stretch range of motion
                                    (ROM) and represented the calf
                                    MTU length extensibility.
                                    Bisecting the angular change
                                    defined the first half and the
                                    last half of the full, defined
                                    stretch ROM.
Passive elastic stiffness (PES)    Ratio of the change in the
                                    passive resistive torque
                                    [[Delta]PRT) to the change in
                                    the ankle angle ([Delta]A), or
                                    [Delta]PRT/[Delta]A. The average
                                    passive elastic stiffness was
                                    calculated for the full stretch
                                    ROM (angular change) and for the
                                    first half and the last half of
                                    the full stretch ROM.

The Kin-Com ASCII data files were transferred to floppy disks, and passive curves within the full stretch ROM were approximated using a third-order polynomial function ([Y=a + [b.sub.1]X + [b.sub.2][X.sup.2] + [b.sub.3][X.sup.3], where Y was the passive torque, X was the angular displacement, and a through [b.sub.3] were constants). From the fitted curve, the change in the PRT ([Delta]PRT) was differentiated at 0.5-degree intervals ([Delta]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 ([Delta]PRT/[Delta]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 ([r.sup.2]=.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, the passive 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 [+ or -] 1.2 degrees, respectively. The ICC and SEM for measuring the maximal PRT were .90 and [+ or -] 3.9 N [multiplied by] 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-Cam 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. [is less than or equal to] 05.

Results

Diagrams of the angular change between the initial dorsiflexion angle and the maximal dorsiflexion angle for the younger, middle-aged, and older women are presented in Figure 1. The passive curves for this full, defined stretch ROM are depicted in Figure 2.

[Figures 1-2 ILLUSTRATION OMITTED]

The MANOVA results indicated a group effect among the 6 dependent variables (F=5.15; df=12,148; P [is less than] .001). Descriptive statistics, 95% confidence intervals of the mean (CIMs), and separate ANOVA results for the angular variables and the maximal PRT are presented in Table 3. The maximal passive dorsiflexion angle, passive angular change, and maximal PRT decreased with increasing age groups. The maximal passive dorsiflexion angle and maximal PRT were reported elsewhere for a different purpose.[31] Tukey post hoc analyses indicated that the older women had a smaller maximal passive dorsiflexion angle ([bar[X=15.39 [degrees], SD=5.78 [degrees]) compared with the younger women ([bar]X=25.83 [degrees], SD=5.5 [degrees]) and the middle-aged women ([bar]X=22.75 [degrees], SD=4.38 [degrees]) (P [is less than] .001). The passive angular change for the older women ([bar]X=25.41 [degrees] , SD=9.72 [degrees]) was less than the passive angular change for the younger women ([bar]X=37.75 [degrees] , SD=5.51 [degrees]) and the middle-aged women ([bar]X=32.96 [degrees], SD=7.83 [degrees]) (P [is less than or equal to] .003). The maximal PRT for the older women ([bar]X=12.61 N [multiplied by] m, SD=5.69) also was less than the maximal PRT for the younger women ([bar]X=21.68 N [multiplied by] m, SD=5.33) and the middle-aged women ([bar]X=17.95 N [multiplied by] m, SD=5.43) (P [is greater than or equal to] .002).

Table 3.

Descriptive Statistics and Results of Analysis of Variance for the Maximal Passive Dorsiflexion (DF) Angle, Passive Angular Change, and Maximal Passive Resistive Torque (PRT) for the Younger Women (n=24), Middle-aged Women (n=24), and Older Women (n=33)

                                        [bar]X    SD

Maximal passive DF angle ([degrees])
 Younger women                          25.83    5.51
 Middle-aged women                      22.75    4.38
 Older women                            15.39    5.78

Passive angular change ([degrees])
 Younger women                          37.75    5.51
 Middle-aged women                      32.96    7.83
 Older women                            25.41    9.72

Maximal PRT (N[multiplied by]m)
 Younger women                          21.68    5.33
 Middle-aged women                      17.95    5.43
 Older women                            12.61    5.69

                                          Range      95% CIM(a)

Maximal passive DF angle ([degrees])
 Younger women                         16.00-34.00   23.51-28.16
 Middle-aged women                     16.00-30.00   20.90-24.60
 Older women                           -2.00-27.00   13.35-17.44

Passive angular change ([degrees])
 Younger women                         20.00-46.00   35.42-40.08
 Middle-aged women                     23.00-50.00   29.65-36.26
 Older women                           9.00-45.00    22.25-29.08

Maximal PRT (N[multiplied by]m)
 Younger women                         10.20-31.00   19.43-23.93
 Middle-aged women                     9.20-32.20    15.66-20.24
 Older women                           3.20-25.20    10.60-14.62

                                          Statistical Test

                                       F Ratio   df       P

Maximal passive DF angle ([degrees])
 Younger women                          29.37    2,78   <.001
 Middle-aged women
 Older women

Passive angular change ([degrees])
 Younger women                          16.21    2,78   <.001
 Middle-aged women
 Older women

Maximal PRT (N[multiplied by]m)
 Younger women                          19.49    2,78   <.001
 Middle-aged women
 Older women

(a) CIM = confidence interval of the mean.

Descriptive statistics, 95% CIMs, and separate ANOVA results for the PES within the 3 stretch ROMs are presented in Table 4. The average PES for the last half of the full, defined stretch ROM decreased with increasing age groups, but the average PES for the full, defined dorsiflexion stretch ROM and for the first half of the full, defined dorsiflexion stretch ROM did not differ among the 3 age groups. Tukey post hoc analysis indicated that the average PES was less for the older women ([bar]X=0.59, SD=0.20) than for the younger women ([bar]X=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.

Table 4.

Descriptive Statistics and Results of Analysis of Variance for the Average Passive Elastic Stiffness (in Newton-meters per Degree) (PES) for the Full, Defined Dorsiflexion (DF) Stretch Range of Motion (ROM) and for the First Half and the Last Half of the Full Stretch ROM for the Younger Women (n=24), Middle-aged Women (n=24), and Older Women (n=33)

Statistical Test

                                                   [bar]X     SD

Average PES for the full DF stretch ROM
 Younger women                                      0.50     0.11
 Middle-aged women                                  0.49     0.16
 Older women                                        0.44     0.13

Average PES for the first half of DF stretch ROM
 Younger women                                      0.26     0.07
 Middle-aged women                                  0.30     0.12
 Older women                                        0.29     0.12

Average PES for the last half of DF stretch ROM
 Younger women                                      0.74     0.19
 Middle-aged women                                  0.69     0.21
 Older women                                        0.59     0.20

                                            Range      95% CIM(a)

Average PES for the full DF stretch ROM
 Younger women                            0.27-0.74    0.45-0.55
 Middle-aged women                        0.24-0.83    0.42-0.56
 Older women                              0.20-0.95    0.39-0.48

Average PES for the first half of DF
 stretch ROM
 Younger women                            0.12-0.39    0.23-0.29
 Middle-aged women                        0.11-0.53    0.25-0.35
 Older women                              0.10-0.57    0.24-0.33

Average PES for the last half of DF
 stretch ROM
 Younger women                            0.43-1.18    0.66-0.82
 Middle-aged women                        0.38-1.17    0.60-0.78
 Older women                              0.26-1.34    0.52-0.66

                                            Statistical Test

                                          F Ratio    df     P

Average PES for the full DF stretch ROM
 Younger women
 Middle-aged women                         1.85     2,78   .165
 Older women

Average PES for the first half of DF
 stretch ROM
 Younger women
 Middle-aged women                         0.65     2,78   .524
 Older women

Average PES for the last half of DF
 stretch ROM
 Younger women
 Middle-aged women                         4.10     2,78   .020
 Older women

(a) CIM=confidence interval of the mean.

Within the last half of the full, defined stretch ROM, the average PES, passive angular change, and change in the PRT for the middle aged women and the older women were expressed as a percentage of the values for the younger women (100%) (Fig. 3). The average PES for the older women was 80% of that of the younger women. The angular change for the older women was 68% of that of the younger women, and the change in the PRT was 56% of that of the younger women.

[Figure 3 ILLUSTRATION OMITTED]

The Pearson correlation coefficients for comparison of age with the measurement variables are presented in Table 5. Age showed negative relationships with the maximal passive dorsiflexion angle (r=-.73), the passive angular change (r=-.55), and the maximal PRT (r=-.55). Age also showed negative relationships with the average PES within the full stretch ROM (r =-.23) and within the last half of the full stretch ROM (r = -.33).

Table 5.

Pearson Product-Moment Correlation Coefficients for Comparison of Age With Maximal Passive Dorsiflexion (DF) Angle, Passive Angular Change, Maximal Passive Resistive Torque (PRT), and Average Passive Elastic Stiffness (PES) for the Full, Defined Stretch Range of Motion (ROM) (Full) and for the First Half (First) and the Last Half (Last) of the Full Stretch ROM for All Women Combined (N=81)

          Maximal Passive        Passive Angular      Maximal PRT
          DF Angle ([degrees])   Change ([degrees])   (N [multiplied
                                                       by] m)

Age (y)   -.73(a)                -.55(a)              -.55(a)

          Average PES (N [multiplied by]/[degrees])

          Full      First   Last

Age (y)   -.23(c)   .04     -.33(b)

(a) P<.001.

(b) P=.002.

(c) P<.05.

Discussion

The shape of the passive curves within the full stretch ROM that was common among the 3 groups appeared similar. The curves for the middle-aged and older women appeared truncated in relation to the curves for the younger women because they had less maximal passive dorsiflexion ROM and less PRT at their maximal limit. The initial dorsiflexion angles for the curves, however, were similar among groups (Figs. 1 and 2). The curves were superimposed to illustrate their similarities (Fig. 4). The similarity of the curves within their common ROMs suggested that the PES within this ROM may not differ among groups. To examine this possibility and to compare our results with the results from a previous study,[5] we determined the PES at 0, 5, 10, and 15 degrees of dorsiflexion for the available curves within these angles. The descriptive statistics for the PES at the 4 angles are presented in Table 6. A 2-way ANOVA for repeated measures indicated an increase among the 4 angles with greater dorsiflexion (F=292.85; df=3,189; P[is less than].001), but no group effect and no interaction effect.

[Figure 4 ILLUSTRATION OMITTED]

Table 6.

Descriptive Statistics for Passive Elastic Stiffness (in Newton-meters per Degree) at 0, 5, 10, and 15 Degrees of Dorsiflexion (DF) Within the Range of Passive Stretch Common to the Younger Women, Middle-aged Women, and Older Women(a)

                                [bar]X    SD      Range

0 [degrees] of DF stretch
  Younger women (n=24)          0.32     0.10   0.18-0.49
  Middle-aged women (n=24)      0.32     0.09   0.19-0.53
  Older women (n=28)            0.39     0.19   0.13-1.08
5 [degrees] of DF stretch
  Younger women (n=24)          0.42     0.13   0.23-0.65
  Middle-aged women (n=24)      0.43     0.13   0.28-0.71
  Older women (n=31)            0.47     0.23   0.20-1.36
10 [degrees] of DF stretch
  Younger women (n=24)          0.54     0.16   0.30-0.84
  Middle-aged women (n=24)      0.56     0.17   0.36-0.95
  Older women (n=29)            0.59     0.26   0.28-1.54
15 [degrees] of DF stretch
  Younger women (n=24)          0.67     0.18   0.39-1.06
  Middle-aged women (n=24)      0.70     0.22   0.43-1.33
  Older women (n=20)            0.71     0.25   0.38-1.16

(a) Passive elastic stiffness was not significantly different among the 3 age groups.

The differences among age groups that we observed may have been influenced by structures other than the calf MTU. Changes in the ankle joint capsule associated ligaments, fascia, and the skin also could have contributed to the age group differences. Isolating the relative contributions of the different tissues to the variables that we measured was beyond the scope of our study. We believe, however, that the calf MTU contributed the primary PRT and PES to the passive stretch, particularly because the maximal passive dorsiflexion stretch was defined separately for each subject and the 2-joint gastrocnemius MTU was lengthened with the knee fully extended. Within the calf MTU, the calf muscle tissue and the associated connective tissues (epimysium, perimysium, and endomysium) were probably the main tissues lengthened; tendons are considered very stiff and do not contribute much to the extensibility of the MTU.[32-34] Calculating the average PES through the full, defined dorsiflexion stretch ROM and to the point of maximal available passive dorsiflexion allowed us to make what we believe are valid age group comparisons based primarily on the maximal stretch ROM tolerated for each subject.

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.[1-4] 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.[35-39] 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 units[11-16] and muscle mass and force.[14-16,19,21] 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 units[11-16] and a decrease in the number[15-17,18] and size[15,17-21] 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 [Delta]PRT/[Delta]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 Vandervoort[5] 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 al[6,7] 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,[2-5-8] although our results also support previously published reports.[3-5]

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.[15,23-25] Based on the results of studies of the connective tissue arrangement of the perimysium of skeletal muscles,[41-43] 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 neuropathies[45] or central nervous system deficits[46] 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

Our results demonstrated that the maximal passive dorsiflexion angle, passive angular change, maximal PRT, and average PES within the last half of maximal available stretch ROM of the calf MTU were decreased for older women compared with younger women. These findings suggested that the calf MTUs of the older women were shorter with less passive length extensibility. Age was negatively associated with the maximal passive dorsiflexion ROM (maximal calf MTU length), passive angular change (calf MTU passive length extensibility), maximal PRT, and the average PES within the last half of the maximum available full, defined passive stretch ROM for active women.

(*) Chattecx Carp, 101 Memorial Dr, PO Box 4287, Chattanooga, TN 37405.

([dagger]) Therapeutics Unlimited Inc, 2835 Friendship St, Iowa City, IA 52245.

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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) ([e-mail]). 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.

Concept, research design, writing, data analysis, and fund procurement were provided by Gajdosik, Vander Linden, and Williams; data collection, by Gajdosik and Vander Linden; project management and subjects, facilities/ equipment, institutional liaisons, and clerical/secretarial support, by Gajdosik. Dr Kathleen Miller, Professor and Associate Dean, School of Education, The University of Montana, assisted with the statistical analyses. Lori Bushway and Brian Heuiser provided technical assistance. Peter McNair, PhD, Member of the New Zealand College of Physiotherapy, and Associate Professor, School of Physiotherapy, Auckland Institute of Technology, New Zealand, developed the software programs used to differentiate the passive elastic stiffness data.

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.

This article was submitted May 20, 1998, and was accepted June 9, 1999.3