Age and passive ankle stiffness in healthy women.

Age and Passive Ankle Stiffness in Healthy Women In the United States and Canada, health surveys have demonstrated that the elderly segment of the population has the highest proportion of physical disability [1] and that stiff joints can be a major cause of this problem. [2] Trichard et al surveyed 100 elderly subjects over the age of 60 years and found complaints of moderate to severe joint stiffness in 70% of the sample. [3] In another health survey, arthritis and rheumatism (two clinical conditions where complaints of joints stiffness are common) were the most frequent ailments to be reported, especially for women. [4] By the year 2030, the elderly in North America will comprise 18% to 20% of the total population, with the majority of this group comprised of women. [15] Although physical therapists commonly treat patients with joint stiffness in the clinical setting, information on the normal levels of mobility to be expected at joints of people of different ages is limited; hence, clinical methods aimed at assessing and improving joint stiffness are difficult to extrapolate to the elderly.

Because the ankle joint complex has an important role in gait, [6] posture control, [7] and many activities of daily living, it is particularly important to understand the relationship between age and passive stiffness in this articulation. For example, although Murray observed that elderly men exhibited less ankle dorsiflexion (DF) at the beginning and end of the stance phase of the gait cycle, [8] it is not known whether this reduction was caused by an age-related increase in passive resistance or a decrease in dorsiflexor muscle strength, or both. The observation that portural sway is age dependent [7,9] may be important in this regard. Instantaneous center of pressure, one of the primary variables evaluated in postural sway studies, is believed to be representative of the muscular moment of force about the ankle joint. [7] To the extent that passive ankle joint or muscle stiffness relates to a muscle's active ability to generate torque, the role of this joint in postural control and functional activities could possibly be affected. The relationship between muscle force production and passive ankle joint stiffness remains unclear and has not been quantified in the elderly.

Joint stiffness often refers to a subjective complaint in the clinical setting, but it can also be measured objectively. [10] By measuring the resistive torque throughout the range of motion and plotting this value against the angular displacement, a torque-versus-displacement curve can be generated, and variables describing joints stiffness can be identified at preselected angular displacements. [11-13] Figure 1 illustrates two such variables relevant to this study: passive torque and passive elastic stiffness at x degrees of DF. The advantage of measuring joint stiffness as compared with ROM is the quantification of mechanical properties throughout the ROM being investigated. [14] Research on joint stiffness can basically be divided into studies of normal reflexogenic mechanisms [15,16] with clinical investigations of neurologically impaired patients [17,18] and studies of passive joint stiffness on healthy subjects and patients with rheumatic disorders. [11] In vivo studies suggest that a major portion of passive stiffness observed during testing arises from the passive elongation of muscle, tendon, and joint capsule [11,19] with the primary resistance arising from a length change in the muscle belly. [20-22] This finding appears to be supported by in vitro studies as well. [23-26]

Abnormal intra-articular stiffness is believed to be a result of changes in the mechanical and biochemical properties of collagen, [27-29] and similar changes in the connective tissue of muscle are believed to occur as well. [30,31] One physiological theory of aging described by Hayflick [32] proposes that molecular cross-linking in collagen molecules increases with age itself, thereby altering the mechanical characteristics of collagen at the cellular level. Both in vitro [33,34] and in vivo [19,35] studies of the mechanical properties of joints have relied on the cross-linkage theory to explain their age-related findings of increased stiffness.

To date, studies regarding age and passive stiffness have been conducted on finger, [11,35-38] knee, [39] and elbow [40] joints, with reports of an age-related increase in passive stiffness in the finger and knee joints only. [11,35-39] Several articles have reported passive stiffness values for normal ankles of young adult subjects, [13,15,18,41-43] but there is no literature pertaining to the influence of age. The purpose of this study, therefore, was to obtain values for passive torque and passive elastic stiffness during ankle DF in young (aged 21-40 years), middle-aged (aged 41-60 years), and young elderly (aged 61-80 years) women. The research hypothesis was that there would be a significant difference between young, middle-aged, and elderly women in measurements of passive ankle joint stiffness.

Because changes in gastrocnemius muscle length have been shown to occur as a result of changes in both ankle and knee joint position, [25-27] a secondary part of the study used the knee in 90 degrees of flexion, or knee-flexed (KF), and knee in full extension, or knee-extended (KE), testing positions to quantify the effect of knee joint angle on ankle joint stiffness. The secondary research hypothesis, therefore, was that there would be a significant difference between measurements of passive ankle joint stiffness in the KF and KE positions. An important underlying assumption was that the resistance to passive movement at the subtalar joint and remaining intertarsal joints would not be evaluated separately from the talocrural joint and therefore would be a contributing factor to passive ankle joint stiffness.

Method

Subjects

Forty-five healthy, female, Caucasian volunteers, aged 21 to 77 years, were recruited from the community and evaluated in the study. Subjects were grouped according to preset age categories of young, middle-aged, and young elderly. Descriptive statistics for age, height, and weight characteristics are presented in Table 1. To be included in the study, subjects had to indicate through a medical history that they were medically stable from a cardiorespiratory perspective. In addition, they were required to 1) be functionally independent with no history of medical treatment for an orthopedic, rheumatological, or neurological injury to the back or lower extremity; 2) exhibit more than 10 degrees of passive plantar flexion (PF) and 10 degrees of passive DF at the ankle joint in both the KF and KE positions; and 3) be capable of maintaining two-point kneeling and prone-lying postures for five minutes during the testing period.

Measurement System

The torque motor system [14] used in this study was designed to passively move the ankle joint through a predetermined range of PF and DF. The experimental apparatus is illustrated in Figure 2. A strain gauge incorporated into the leverage system of the footplate recorded the resistive torque, and the angular displacement was monitored with a potentiometer. Both the passive elastic stiffness (slope) at x degrees of DF and passive torque at x degrees of DF were derived with custom-made software (*1) after analog-to-digital conversion (*2) and storage on the laboratory microcomputer. (*3) [11] electromyographic activity from the lateral head of the gastrocnemius muscle and the central portion of the soleus muscle was monitored using 9-mm DISA surface electrodes (*4) attached to skin prepared by alcohol swabs. A high-gain amplification using a Dantec 15CO1 EMG amplifier (*4) allowed detection of very slight muscle contractions. No trials produced EMG activity during testing.

We have previously evaluated the reliability of the system [14] and obtained an intraclass correlation coefficient ([r.sub.1]) [44] of .994 for repeated testing of known static torques. Reliability of dynamic measurement of ankle joint stiffness was also determined on two consecutive days with 10 subjects. Passive stiffness was evaluated at 0 (neutral), 5, and 10 degrees of DF. The reliability values for passive torque ranged from .767 to .943 for the three ankle joint positions in both testing positions and thus exceeded the minimum value of .75 for acceptable reliability. [45]

Subject Positioning

The subjects were tested in the prone-lying posture in KE and in the two-point kneeling posture in KF. We used a firm but adjustable treatment table, (*5) which was helpful when positioning the elderly subjects in the ankle testing unit and facilitated the alignment of the ankle axis of rotation with that of the footplate. A line passing between the distal extent of the malleoli was defined as the axis of rotation. [46] Sequence of test positioning and the limb to be tested were determined randomly.

Evaluation Procedure

All testing was performed in the Neuromuscular Integration Laboratory at the Department of Physical Therapy, University of Western Ontario, London, Ontario, Canada. Room temperature was controlled to within 70 [degrees] to 80 [degrees]F. Upon arrival, the purpose and nature of the study were explained to the subjects. After reading the Information for Participants Document, written consent was obtained. All candidates were screened to ensure that they were medically suitable and met all inclusion criteria. Information regarding activity level was obtained through questionnaire format. Subjects were asked whether they exercised and, if so, the frequency (days per week) and type of activity (walking, running, sports, fitness, other).

Each subject was screened for adequate ankle ROM prior to testing. With a full squat, ROM in the KF position was measured. By stretching the ankle plantar flexors in standing, ROM in the KE position was determined. A gravity-referenced goniometer aligned with the shaft of the fibula was used to demonstrate that the ankle joint was capable of moving well beyond the test ROM in the two testing positions. The EMG surface electrodes were attached to the lateral gastrocnemius and soleus muscles. The subject assumed one of the test positions, and the tested ankle was placed securely in the ankle testing unit. Adequate foot fixation was achieved with the use of an adjustable heel stop on the calcaneus. The proximal dorsal foot strap was positioned in the area of the talar head and helped to secure the hindfoot in the heel stop. Stabilization of the midtarsal joints and the metatarsals was provided by the distal dorsal foot strap. From the starting position of 10 degrees PF, the ankle was cycled passively through a 20-degree test ROM to 10 degrees of DF at 6 [degrees]/sec. A slow velocity was used because no EMG activity occurs during stiffness tests on healthy ankle joints at velocities less than 20 [degrees]/sec. [13] The test continued uninterrupted for six complete cycles, with each cycle defined as a change in position from 10 degrees of PF through the neutral position to 10 degrees of DF and back to 10 degrees of PF. Total time of testing in the two positions was approximately five minutes.

Data Analysis

Using the custom-made software, the data were analyzed by averaging the last five cycles of the test ROM. The first cycle was eliminated because it was considered an acclimatization cycle. [13] The resultant torque-versus-displacement curve was generated by fitting the data with a fourth-order polynomial equation (Y = [ax.sup.4] + [bx.sup.3] + [cx.sup.2] + dx + e, where Y is the passive torque, x is the angular displacement, and a through e are constants) from which the values for passive torque (in newton-meters) and passive elastic stiffness (in newton-meters per degree) at x degrees of DF were obtained. Passive elastic stiffness describes the slope of the curve and was derived from the polynomial equation (dy/dx = [4ax.sup.3] + [3bx.sup.2] + 2cx + d, where dy/dx is passive elastic stiffness). Data analysis was based on the mean values for passive torque and passive elastic stiffness at 0, 5, and 10 degrees of DF for the two testing positions in the three age groups. Only ankle movement into DF was analyzed because restrictions of DF are more commonly seen in the clinical environment and little or no passive elastic stiffness has been found at the ankle joint in PF positions. [42,43] Differences in passive torque and passive elastic stiffness were assessed according to grouping factors of age, knee, and ankle position with the analysis of variance (ANOVA) design for repeated measures on the latter two factors. Because homogeneity of variance is an underlying assumption for the use of the ANOVA procedure, probability values were adjusted according to the Greenhouse-Geisser procedure when groups had nonhomogenous variances. The Newman-Keuls statistic was used for post hoc comparisons between mean values. [44] All statistical analyses were performed with BMDP statistical software. (*6)

Results

The age group means and standard deviations for passive torque and passive elastic stiffness are displayed in Tables 2 and 3, respectively. Passive torque values increased nonlinearly across all age groups in both testing positions as the ankle moved further into DF. This nonlinear change was reflected by increases in the passive elastic stiffness as the ankle was dorsiflexed. Figure 3 illustrates that the variability of these measurements was greater both through the test ROM and in the young elderly age group. For example, standard deviations for passive torque at 10 degrees of DF in the KF position were 26%, 43%, and 51% of the mean for young, middle-aged, and young elderly age groups, respectively. In the KE position, the values were 20%, 29%, and 36% of the mean, respectively. A similar trend was evident for passive elastic stiffness at 10 degrees of DF. In the KE position, the standard deviations were 43%, 65%, and 64% of the mean for the three age groups, and the KE values were 28%, 40%, and 51% of the mean, respectively.

The results of the ANOVA are presented in Tables 4 and 5 for passive torque and passive elastic stiffness, respectively. The ANOVA revealed no significant difference in passive torque or passive elastic stiffness between the age groups tested or between testing positions. Interaction between factors was also nonsignificant. Differences in passive torque and passive elastic stiffness values were significant between each of the three ankle positions examined.

Discussion

Age

We found no significant difference in passive torque or passive elastic stiffness at the ankle joint between the age groups tested. This finding does not support the trend of an increase in these variables, as reported in the literature reviewed in the introduction. The limited volume of research focusing on the relationship between age and passive joint stiffness has been directed primarily toward finger joint evaluation and suggests that passive elastic stiffness increases with age. [11,35-38] For other joints, Such et al found a significant increase with age in their study of knee joint stiffness, [39] whereas Wiegner and Watts found no correlation with age in their study of passive elbow stiffness. [40] If an age-related increase in passive joint stiffness does exist, it may be joint specific. Because some reports have used different methodologies [36,37] or only presented qualitative data [11] and others have missing age groups in their sample, [35,38] the relationship between passive stiffness and age remains unclear.

The trend of increasing variability throughout the test ROM, as well as in the older age groups, could mask any true difference that might exist between the age groups. Probability values, however, were high and thus supported the conclusion that the values across age groups were equivalent. Variability in the joint stiffness measurements of healthy young subjects appears to be quite large. Hufschmidt and Mauritz reported a standard deviation for passive torque at 10 degrees of DF that was 44% of the mean. [13] Weiss et al found standard deviations that were 29% to 35% of their mean passive stiffness measurements. [43] In our study, the increase in variability with age was quite marked. The importance of this finding is that future clinical trials of treatment efficacy must adjust sample size estimations according to the age of the patients involved.

Wright has suggested that limb dominance, occupation, race, activity level, and pre-evaluation warm-up may affect ROM values. [47] Because passive torque is related to joint position, these factors may also affect joint stiffness measurements. It is unlikely, however, that limb dominance could have significantly affected our results because similar numbers of left and right ankles were tested. All subjects were Caucasian in racial origin; therefore, the race of the sample was homogeneous. Occupation was not specifically evaluated, and its effect on the age relationship is therefore unknown. It is unlikely, however, that any of the women were in a high-risk occupational category for ankle joint deterioration.

With regard to activity level, in our study a larger percentage of the young group (86.6%) was physically active, but a majority of the young elderly age group (66.7%) reported that they also exercised regularly. If increased activity levels decrease joint stiffness values, as suggested by Chapman et al, [35] then relatively low stiffness would be expected in this sample of active senior citizens. The values from this study should be compared to those of a sedentary, institutionalized group of elderly women in whom stiffness might well be increased, because our profession also assesses their joint function routinely.

During our actual testing sessions, the activity level was closely controlled. All subjects performed the ROM screening test and rested in the same position during EMG surface electrode application. Activity level prior to the testing session, however, was not controlled, and its effect on the joint measurements is unknown. Increased activity may warm the joint structures, and Wright has shown that an increase in joint temperature will decrease mechanical joint stiffness 10% to 20%, depending on the joint studied and the method of heating. [10] Variability in pre-evaluation activity level, as well as the laboratory temperature itself, therefore, could possibly contribute to the variability in the measurements and mask any age-related differences. We are unaware, however, of any investigations that demonstrate changes in passive stiffness values in healthy subjects as a result of minor alterations in room temperature. In this study, the laboratory environment did not appear to be different for any one age group, and it is unlikely to explain the lack of an age relationship with the passive stiffness measurements.

Diurnal variation in joint stiffness is a common clinical complaint and has been suggested to be another factor affecting the objective measurement of joint resistive torque. [48] In our study, all except three subjects were tested in the afternoon. We, therefore, do not believe that this factor would significantly affect our results.

A possible reduction in muscle volume or calf cross-sectional area may explain the lack of an age relationship and the increased variability with age. Hufschmidt and Mauritz found that passive torque at 10 degrees of DF was significantly related to calf cross-sectional area, with a moderate positive correlation coefficient (r = .506). [13] Wiegner and Watts found a stronger relationship (r = .76) between passive elbow joint stiffness and upper arm volume. [40] Such et al found that both knee joints and thighs with a large circumference exhibited greater amounts of passive torque than smaller ones. [39] The three age groups in this study demonstrated similar mean heights. The middle-aged and young elderly age groups were about the same mean weight but were heavier than the younger subjects. Vandervoort and McComas, however, have found that in comparisons of young and elderly adults of similar size, the cross-sectional areas of the triceps surae muscle decreased with age, as did PF and DF muscle strength. [49] The ratio of passive stiffness to muscle size and strength, therefore, may increase in the elderly. As a result, following middle age it would take a larger proportion of total muscle strength to move the ankle actively through the ROM.

Passive stiffness has been shown to be relatively minor and stable when the ankle is near the neutral position and to increase when the ankle is moved out of mid-range. [43] Because our observations were made in this functional range where the joint rotates repetitively during gait, it is possible that any differences attributable to the aging process were too subtle for detection. If an age-related difference does exist in a more dorsiflexed position, we believe that the increase in passive joint stiffness in older age groups must occur quite dramatically when the foot is past the 10-degree DF position.

Knee Position

No significant difference in passive torque or passive elastic stiffness at the ankle joint occurred between the two knee positions tested. Sale et al have shown with radiographs that the gastrocnemius muscle would be lengthened by approximately 0.5 cm as the knee of a tall male subject is moved from full flexion to full extension. [50] Ankle rotation from the neutral to the 10-degree DF position would have a similar effect on the length of the gastrocnemius muscle belly when the knee is extended [21] and just 6% less stretch if the knee is flexed. [51] Any difference in passive ankle joint stiffness measurements attributable to a change in knee joint position may not occur from such a small change in muscle length, unless the ankle is moved further into DF where the gastrocnemius muscle is in a steeper portion of its passive stiffness curve.

Conclusions

Passive torque and passive elastic stiffness values during DF increased significantly between the 0-, 5-, and 10-degree DF positions in a nonlinear manner, with no age-related differences. This latter finding may be an accurate representation of a healthy female population in which all age groups are active. Alternatively, the lack of an age relationship may be due to bias stemming from the cross-sectional design of this study of volunteers. The variability of both stiffness measurements increased with age and with angular displacement. It is unlikely, however, that any age relationship was obscured, because mean values of the three age groups were generally very similar. Greater variability may very well be an age-related phenomenon itself.

We found no difference between the KF and KE testing positions in the passive stiffness measurements during DF to 10 degrees. The length change in the gastrocnemius muscle attributable to the change in knee position did not appear to make a significant difference in its resistance to passive movement at the ankle joint.

The results of our study, therefore, do not support the theory that increasing joint stiffness is an age-dependent phenomenon. Even though decreases in contractile tissue occur with aging, the noncontractile tissue about the ankle joint does not seem to exhibit similar changes in the mechanical behavior within the functional ROM. Further study is needed to clarify the interrelationships between age, joint stiffness, muscle strength, and active ROM.

Acknowledgments

We thank Bob Kager, University of Western Ontario Mechanical Engineering Shop, and Dr Conrad Yim, CY Software, for their technical assistance in this project, and Helen Cheung of the University of Western Ontario Biostatistical Support Unit.

(1) CY Software, London, Ontario, Canada N6H 4V3.

(2) DT2801 A/D Conversion Board, Data Translation Inc, Marlborough, MA 01752.

(3) Z-151 PC, Zenith Data Systems, Benton Harbor, MI 49022.

(4) DISA Dantec Elektronik, Skovlunde, Denmark, DK-2740.

(5) Cardon Mobilization Table R28535, Cardon Rehabilitation Products, 3206 Wharton Way, Mississauga, Ontario, Canada L4X 2C1.

(6) Biomedical Data Processing Statistical Software, 1440 Sepulveda Blvd, University of California at Los Angeles, Los Angeles, CA 90025.

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B Chesworth, MClSc(PT), is Physical Therapy Clinical Associate, University Hospital-University of Western Ontario Physical Therapy Clinic, University of Western Ontario, London, Ontario, Canada N6G 1H1. Address correspondence to Mr Chesworth at UH/UWO, PT Clinic, Elborn College, University of Western Ontario, London, Ontario, Canada N6G 1H1.

A Vandervoort, PhD, is Assistant Professor, Department of Physical Therapy, Faculty of Applied Health Sciences, University of Western Ontario.

This study was supported by grants from the Gerontology Research Council of Ontario, the Jal Tata Research Fund of the London District, Ontario Physiotherapy Association, and the Academic Development Fund of the University of Western Ontario.

This article was adapted from a presentation given at the American Physical Therapy Association-Canadian Physiotherapy Association Joint Congress, Las Vegas, NV, June 8-20, 1988.

This article was submitted May 5, 1988; was with the authors for revision for six weeks; and was accepted October 26, 1988.