Information from the sensory systems is important for postural control. Normally, somatosensory, visual and vestibular inputs are available to detect a person’s postural orientation and equilibrium with respect to the environment and gravity (7). However, studies show that deterioration of the sensory systems affects the postural stability and the ability to recover from a loss of balance. Indeed, poor postural stability has been identified as a major intrinsic factor that causes falls in the elderly (14).
In the absence of vision, the detection of limb position and movement is termed “limb position sense” and “kinesthesia,” respectively, which is known collectively as “limb proprioception” (4). It is mediated by cutaneous receptors in the skin and proprioceptors in muscles, tendons, ligaments, and joints, which signal to the central nervous system both the stationary position of a limb and the speed and direction of its movement. Limb proprioception has been found to diminish with age. Hurley et al. (9) found that elderly subjects, with a mean age of 72 yr, made significantly larger errors than did young subjects in an active knee repositioning test. Our earlier study (30), further showed that the joint detection threshold was 50% higher in older subjects (aged 57–77 yr) than in subjects aged 25–35 yr, for both knee flexion and extension.
As would be expected, elderly fallers were found to have significantly reduced proprioception in their lower limbs (14). In view of the high medicare cost consequent to falls, it becomes important to determine whether exercise could help improve limb proprioception in the elderly. In this connection, Tsang and Hui-Chan (24) conducted a cross-sectional study and found that elderly practitioners of Tai Chi, a Chinese mind-body exercise, achieved significantly better acuity in knee proprioception sense, in that they showed smaller knee angle errors in a passive knee repositioning test when compared with those of control subjects similar in age, gender, and physical activity level. However, it is not known whether the improved joint proprioception is comparable to that in young, healthy subjects.
In terms of postural control, Tsang et al. (25) have demonstrated that elderly Tai Chi practitioners could attain the same level of balance performance in a sensory organization test (SOT) as that of young, healthy subjects, when standing under reduced or conflicting somatosensory, visual, and vestibular conditions. In another study, Tsang and Hui-Chan (24) chose a more dynamic standing balance assessment using the limits of stability (LOS) test and showed that elderly Tai Chi practitioners improved their balance more than that of control subjects similar in age, gender, and physical activity level. Whether the improved control of the more dynamic LOS test is comparable to that of young subjects is still unknown. Therefore, the first objective in the present study was to examine whether male elderly Tai Chi practitioners have developed knee joint proprioception and the control of their LOS comparable to those of young subjects.
In the aforementioned cross-sectional studies (24,25), we surmised that the improved knee joint proprioception and balance performance in SOT and LOS of elderly Tai Chi practitioners could be attributed, at least in part, to the repeated practice of Tai Chi for ≥ 1 yr. This is because Tai Chi puts great emphasis on the exact joint position and limb direction. It also involves precisely controlled weight transfer in double leg stance, and controlled weight shifting between double and single leg stance, in a smooth and coordinated manner (26). The improvement in balance control by Tai Chi is supported by our prospective study in which the elderly subjects received 8 wk of intensive Tai Chi training had improved significantly in balance control, in terms of: 1) less body sway when standing under conditions requiring an increased reliance on the vestibular system and 2) more smooth shifting of their weight to different directions within their base of support (8). However, is improvement in knee joint proprioception and LOS specific only to Tai Chi training? What about other sports such as golf? Like the practice of Tai Chi which is popular among elderly Chinese, golf is a Western sport that is also popular among elderly Westerners, and increasingly so among the Asian population. It requires concentration of mind, as well as precise and coordinated trunk and arm movements in order to hit the golf ball accurately (19). Consequently, experienced golfers could also have improved joint proprioception and balance control. Thus, the second objective of the present study was to compare the knee joint proprioception and LOS of the golfers with those of elderly Tai Chi practitioners and healthy subjects matched for age, gender, and physical activity level, as well as with those of young healthy subjects. Finally, because joint afferents are known to contribute to the control of balance (7), our third objective was to investigate whether any relationship existed between knee joint proprioception and limits of stability during voluntary weight shifting in these three groups of male elderly subjects.
Subjects and Study Design
Thirty-five male community-dwelling elderly subjects, aged 60 or older participated in this study. Twelve of them were Tai Chi practitioners (mean age = 69.6 ± SD 5.7 yr) recruited from local Tai Chi clubs. All had practiced Tai Chi for a minimum of 1.5 h·wk−1 for at least 3 yr (mean Tai Chi experience = 8.4 ± 9.1 yr). Eleven were golfers (mean age = 66.2 ± 6.8 yr) recruited from local golf clubs. All had practiced golf for the same minimum amount of 1.5 h·wk−1 and the same minimum duration of at least 3 yr (mean golf experience = 15.2 ± 13.4 yr). Twelve were elderly control subjects (mean age = 71.3 ± 6.6 yr) recruited from several community elderly centers. They had no previous experience in either Tai Chi or golf, though some took morning walks or did stretching exercises.
All the subjects could walk without the assistance of walking aids. Those candidates reported history of falls in the previous 12 months were excluded. A fall is defined as an event resulting in a person inadvertently coming to rest on the ground or another lower level. Major intrinsic events, e.g., seizure, and overwhelming external forces, e.g., motor vehicle accident will be excluded. All subjects were able to communicate and were active enough to comply with the testing procedures. All were independent in their activities of daily living at the time of the study. Candidate subjects showing symptomatic cardiovascular diseases when subjected to moderate exertion were excluded. Also excluded were candidates with poorly controlled hypertension or symptomatic orthostatic hypotension, severe cognitive impairment, Parkinson’s disease, stroke or any other neurologic disorder, peripheral neuropathy of the lower extremities, and disabling arthritis or metastatic cancer.
Twelve young healthy subjects (mean age = 20.3 ± 1.4 yr) were also recruited. All were male university students who exercised regularly for at least 2 h·wk−1. Exclusion criteria were the presence of inner ear problems, dizziness, long-term medication, a history of injury within 1 yr before the study, prior orthopedic operation, or neurologic disease.
The elderly candidates were first screened using a general health questionnaire and a physical activity questionnaire. The validated Chinese version of the Mini-Mental Status Examination of Folstein et al. was then administered (3). The scale ranges from 0 to 30. A score below 24 was considered indicative of cognitive dysfunction, and such subjects were excluded from this study. The physical activity level questionnaire was a modified version of the Minnesota Leisure Time Physical Activity Questionnaire (28). It had been used in our previous studies (24,25) and was used in the present project to compare physical activity levels among the three elderly groups in terms of their metabolic equivalent (MET) status. These protocols were approved by the Ethics Committee of the Hong Kong Polytechnic University, and written informed consent was obtained from all subjects.
Passive knee joint repositioning test.
General methods for testing joint proprioception include: 1) testing the threshold for detecting joint movement, 2) joint position matching with the contralateral limb, and 3) limb segment repositioning called the “joint repositioning test,” all of which could be tested in either a passive or an active mode. Knee joint repositioning test was adopted because the practice of Tai Chi and golf both put great emphasis on exact joint positioning of the knee, which could have improved the acuity of knee joint repositioning, as was already demonstrated in our Tai Chi study (24). Also, some investigators noted that the knee joints are often held in some degrees of flexion during certain functional activities performed by the elderly subjects (9). Others had chosen knee joint proprioception to correlate with selected functional activities in the elderly people (9,14). The test was performed passively in a nonweight-bearing condition. The reason for using a passive and nonweight-bearing protocol in the joint repositioning test was to minimize the motor contribution, which has been found to aid proprioceptive acuity (1).
Using our particular experimental paradigm, we had reported previously that the passive knee joint repositioning test produced highly repeatable data, with intraclass correlation coefficients of 0.90 (24). This paradigm was adopted in the present study and will be briefly described below. The dominant leg that the subject used to kick a ball was tested. The subject sat on the chair of a Cybex Norm dynamometer (Cybex International Inc., Ronkonkome, NY), with the hips fixed in 60° of flexion. The seating position was adjusted so that the edge of the seat was 4–6 cm from the popliteal fossa of the knee. This ensured that the subject’s cutaneous sensation was minimized. An air splint at an air pressure of 20 mm Hg was applied to the tested ankle, to further minimize the influence of cutaneous (e.g., pressure) input. The leg to be tested was positioned such that the rotation axis of the dynamometer’s knee adaptor was in line with that of the subject’s knee joint, defined using the lateral femoral epicondyle. A malleable electrogoniometer (Penny and Giles Biometric Ltd., type XM180, Blackwood, UK) was then attached to the lateral aspect of the knee. The proximal attachment of the electrogoniometer aligned with the femoral axis between the greater trochanter and lateral femoral epicondyle, whereas the distal attachment was in line with the fibular axis between fibular head and lateral malleolus. The subject was then blindfolded.
For the test itself, the knee was passively moved from the initial position of 30° of knee flexion by 3° of extension, at a constant angular velocity of approximately 3°·s−1. It was then held for 3 s in the target position before being returned passively to the initial position, which was again held for a random interval of 3–8 s to minimize the possibility of subjects using “counting” to return the knee to the target position. The knee was then extended at the same angular velocity as before by either 3° or 6° of extension in a random order, so as to avoid subjects using means other than their proprioception sense to return the knee to the target position. The subject was instructed to press a thumb switch when he perceived that the knee had regained the previous target position. Surface electrodes (NeuroCom International, Inc.) were used to detect electromyographic activity in the thenar eminence muscles (mainly the flexor pollicis brevis) of the subject’s thumb. The onset of the EMG signal indicated the moment when the subject perceived that the knee had regained the target position. The EMG signals from the thumb muscles were monitored real time to ensure a quiet baseline before the subject pressed the thumb switch.
The signals from the electrogoniometer, thumb switch, and EMG were stored (through an A/D card, DataQ® Instruments Inc., type DI-720P) for off-line analysis. Each subject completed three trials. The error with which the subject reproduced the initial position was calculated. The three absolute error values were averaged, and the average value, termed the absolute angle error, was used for comparison across the four groups. These are three reasons for choosing the absolute angle error: 1) The absolute angle error can be regarded as a measure of the overall accuracy of performance. It is the average absolute deviation (regardless of the direction) between the subject’s perceived position and target position of the knee. 2) The absolute angle error has the advantage of having taken into consideration both the deviation from the target position (termed as a constant variable) as well as the variability or inconsistency of subject’s performance (termed as a variable error) (18). 3) Consequently, this outcome measure has been commonly used by other investigators when employing joint position sense test (2,17,24) as we had in a previous study (24).
Limits of stability (LOS) test.
After the knee joint repositioning test, the subjects underwent a dynamic standing balance test that involved voluntary weight shifting to determine their LOS. This test measures the subjects’ ability to voluntarily shift their weight in eight different spatial directions within their base of support. Smart EquiTest® equipment (NeuroCom International, Inc.) was employed to record displacements of the center of pressure (COP) during this test. A detailed description of the testing procedure has been reported in our previous study (24) and is therefore only highlighted here. The COP trajectory with respect to height, termed the “normalized COP,” was used to estimate the sway angle of the center of mass (20). The balance measurement system consisted of dual force plates (one for each foot) and a video screen on which the subject’s current normalized COP was continually displayed. There were eight target positions on the screen, with the normalized COP during quiet stance displayed in the center. The subject was instructed to shift his weight so as to move the normalized COP trace to one of the eight target positions, preselected in a random order, as quickly and smoothly as possible, without moving his feet.
Three outcome measures—reaction time, maximum excursion, and directional control—were used to assess dynamic balance control in the LOS test. We had found these outcome measures to be reliable in a previous study with elderly subjects, with intraclass correlation coefficients equal to 0.82, 0.93, and 0.83 for reaction time, maximum excursion, and direction control, respectively (24). Reaction time was defined as the time from the presentation of a visual stimulus as a response signal to the initiation of voluntary shifting of the subject’s center of mass (COM) toward the target location. Maximum excursion measured the maximum displacement of the normalized COP, within the subject’s theoretical limits of stability and without the subject taking a step to recover balance. Directional control measured the smoothness of the displacement of the normalized COP to the target positions. It compared the amount on-target movement of the normalized COP to the amount of off-target movement (15). The subject’s task was to sway as fast, as smoothly and as far as possible, to one of the eight randomly preselected targets located at 100% of the LOS. For each target position, one trial was performed. The average value from the eight target positions was used to compare among the participating subjects. There were familiarization trials, at least one for each target position before data recording, to ensure that subjects understood how to weight shift to the different target positions.
Data Recording and Analysis
Knee joint repositioning.
The first appearance of an EMG signal from the thenar eminence muscles (mainly the flexor pollicis brevis) was taken to indicate the moment when the subject perceived that the joint angle had reached the target value during the repositioning test. The EMG signals were sampled at 1000 Hz, filtered with a bandwidth of 10–500 Hz, and amplified with a gain of 4048. They were then full-wave rectified.
“The first indication of an EMG signal” was taken to be the moment when EMG activity reached 3 standard deviations above the baseline, to minimize the influence of muscular activities due to anticipation and/or noise from the environment. EMG onset was chosen because large variations had been found in our previous study between EMG onset and the thumb switch signals (24). This approach served to minimize the error that could have arisen from the thumb pressing on the switch at slightly different locations and/or with slightly different forces.
Limits of stability test.
All the data from the Smart EquiTest® were processed, using a second-order Butterworth low-pass filter with a cutoff frequency of 0.85 Hz. The force data were used to calculate the subjects’ center of pressure (COP) during balance control tests.
The reaction time was measured from the appearance of a blue circle in the target position, to the onset of the voluntary shifting of the normalized COP toward the target position. The onset of voluntary shifting was defined as the moment when excursions in the normalized COP first exceeded the peak amplitude of the normalized COP excursions, recorded over a 2-s control period before the presentation of the response signal (15).
The subjects leaned as far as possible toward each of the target positions, which were located at 100% of their LOS. The maximum distance traveled toward each target position was computed from the output of the four sensors attached to the support surface of the Smart EquiTest® machine. The data were used to estimate the maximum body sway angle (θ). The maximum sway angle (θ), calculated with respect to each subject’s height, was then expressed as a percentage of the theoretical 100% sway angles of the eight target positions. The method of calculating θ can be found in the work of Shepard et al. (20) and in the Smart EquiTest® System Operators Manual (15).
The degree of directional control was quantified, in terms of the amount of movement of the normalized COP in the on-target direction (toward the target) compared to that in an off-target direction (away from the target). Its value was computed using the algorithm incorporated into the computerized dynamic posturography equipment. The difference between the amount of on-target movement and that of off-target movement of the normalized COP was expressed as a percentage of the total on-target movement as follows (15,24). EQUATION
A straight-line path would have no off-target movement, and the directional control score would thus be 100%.
One-way analysis of variance (ANOVA) was used to compare age, height, and weight among the four subject groups and Kruskal-Wallis test for the Mini-Mental Status Examination results among the three elderly groups. A chi-square test was applied to compare the physical activity levels among the elderly groups due to its categorical nature. An independent t-test was used to compare the years of experience between the Tai Chi practitioners and the golfers. For between-group comparison of the knee joint repositioning test results, a one-way ANOVA was employed. Multivariate analysis of variance was used to compare the outcome measures recorded with the limits of stability (LOS) test among the four groups. If statistically significant differences were found in the multivariate tests, univariate tests were conducted for each of the outcome measures of the LOS test. Post hoc analysis using Bonferroni’s adjustment was conducted, if a significant difference was found in the univariate test. A Pearson product-moment coefficient of correlation was used to correlate the absolute angle error obtained in the knee joint repositioning test, with reaction time, maximum excursion and directional control of the normalized COP in the LOS test among the three groups of elderly subjects. A significance level (α) of 0.05 was chosen for the statistical comparisons.
Table 1 shows a comparison of age, height and weight among the four male groups. One-way ANOVA showed statistically significant differences between the young subjects and the three elderly groups in age, with no significant differences among the three elderly groups of Tai Chi practitioners, golfers, and control subjects in the post hoc analysis. There were also statistically significant differences in height between young subjects on the one hand, and elderly Tai Chi and elderly control subjects on the other. However, any difference in height would not have affected the comparisons of the limits of stability test among the subject groups, because “sway angle” was used to calculate the outcome measures. There were no statistically significant differences in weight among the four group.
Table 1 provides further comparisons of the demographic data for the three elderly groups. Kruskal-Wallis test showed that the three groups were comparable in terms of Mini-Mental Status Examination (MMSE) scores (P = 0.124). All 35 subjects had MMSE scores above 24, indicating that they had no cognitive impairment (3). Physical activity level was also found to be similar, using chi-square test (P = 0.583). As revealed by the general health questionnaire, none of the elderly were limited in any of their activities. Similarities in these variables meant that they would not have confounded any differences in the outcome measures among the three elderly groups. Note that although the golfers had more years of experience than the Tai Chi practitioners, the differences were not significant (P = 0.168).
Knee joint repositioning test.
Table 2 shows that Tai Chi practitioners and golfers had significantly better knee joint proprioceptive acuity and made less absolute angle errors in the knee joint repositioning test than did the control elderly, being 1.7 ± 1.3°, 1.3 ± 0.7° and 3.9 ± 3.1°, respectively (P = 0.001). Their proprioceptive acuity was actually comparable to that of the young control subjects, being 1.1 ± 0.5° (P > 0.05).
Limits of stability test (LOS).
The multivariate ANOVA indicated a statistically significant overall effect across the three outcome measures for the four subject groups (P < 0.001;Table 2). The univariate tests showed that there were statistically significant differences in the reaction time (P < 0.001), maximum excursion (P < 0.001), and directional control of the normalized COP (P = 0.002) among the four groups. Because statistically significant differences were found in all the univariate tests, post hoc analysis using Bonferroni’s adjustment was conducted for the three outcome measures and revealed the findings below.
Both the Tai Chi practitioners and the golfers achieved faster reaction times when leaning to the different target positions (mean = 0.8 ± 0.1 s, 0.8 ± 0.2 s, respectively;Table 2) than did the elderly control subjects (mean = 1.0 ± 0.3 s; P < 0.05), but their reaction times were still significant longer when compared with those of the young control subjects (mean = 0.5 ± 0.1 s; P < 0.05). For the maximum excursion, both exercise groups were able to lean farther toward the eight target positions within their limits of stability (mean = 92.6 ± 5.5%, 92.9 ± 5.7%, respectively) than the elderly control subjects (mean = 83.2 ± 8.2%; P < 0.05;Table 2). In fact, their improved maximum excursion was comparable to that of the young control subjects (mean = 97.1 ± 3.3%; P > 0.05). Similarly, the Tai Chi practitioners and golfers could travel to the target positions through a smoother pathway (mean directional control = 79.0 ± 4.4%, 78.3 ± 5.4%, respectively) than the elderly control subjects (mean = 70.3 ± 7.3%; P < 0.05;Table 2). This level of improved directional control was again comparable to that of the young control subjects (mean = 79.2 ± 7.0%, P > 0.05). In sum, the male elderly Tai Chi practitioners and golfers attained better control when shifting weights within their limits of stability than the elderly control subjects, with regard to reaction time, maximum excursion, and the directional control of normalized COP. Of interest is that improvements in the latter two outcome measures made their performance comparable to that of the young control subjects.
Correlation of the absolute angle errors with the limits of stability outcome measures.
To determine the relationship between proprioceptive input and a related output (balance control), we correlated the absolute angle errors obtained from the knee joint repositioning test with the outcome measures obtained from the limits of stability test (reaction time, maximum excursion, and directional control) in the three elderly groups, using Pearson’s product-moment coefficient of correlation. Our findings showed that the absolute angle errors were indeed correlated with reaction times (r = 0.427; P = 0.013;Table 3;Fig. 1a). Elderly subjects who exhibited larger knee joint repositioning errors required more time, on average, to initiate a voluntary response in moving their body toward the eight spatial targets. Furthermore, the absolute angle errors were inversely correlated with the averaged values of the maximum excursion to the eight target positions (r = −0.522; P = 0.002;Table 3;Fig. 1b). That is to say, elderly subjects exhibiting larger joint repositioning errors, on average, displayed smaller averaged maximum excursion to the eight test directions. A significant negative correlation was also found between the absolute angle errors and directional control of the normalized COP, as measured by the averaged values in the eight target directions (r = −0.396; P = 0.023;Table 3;Fig. 1c). In other words, elderly subjects with larger absolute angle errors showed less directional control, on average, in shifting their weight toward the eight target positions.
Joint Proprioception Sense and Limits of Stability: Effects of Aging
Joint proprioception sense.
Limb proprioception has been reported to decrease with age, after ligamentous injuries, and in some pathological conditions common among the elderly subjects such as stroke and osteoarthritis. Limb proprioception is known to play an important role in maintaining normal body posture, in generating smooth and coordinated movements, and in motor learning and relearning (4). Elderly fallers showed significantly reduced proprioception of the lower limbs, when asked to match the position of the big toe on each side by extending the knee (14).
In the present study, the elderly control subjects made significantly larger angle errors in the passive knee joint repositioning test (mean = 3.9 ± 3.1°) than did the young subjects (mean = 1.1 ± 0.5°; P < 0.05;Table 2). This result agreed with previous findings that the ability to reproduce knee position deteriorated with increasing age. Barrack et al. (2) compared healthy elderly subjects (average age = 63 yr) with young subjects (25 yr), using an active joint repositioning test with 90° of knee flexion as the starting position. The limb was passively moved at 10°·s−1 to target positions ranged from 5° to 25° of knee flexion. The subjects were then asked to reposition the knee to the target positions actively. The absolute angle errors were 4.6° and 3.6° for the elderly and young subjects, respectively, which represented an increase by 28% in the elderly subjects. Petrella et al. (17) used an active joint repositioning test in a standing position, with target positions ranging from 10° to 60° of knee flexion. The elderly (age range, 60–86 yr) and young subjects (age range, 19–27 yr) attained 4.6° and 2.0° in their absolute angle errors, respectively, which represented an increase by 130% in the elderly group. Using a passive knee repositioning test protocol in this study, we detected an even more significant increase (by 255%) in the absolute angle error of elderly control subjects when compared with that of the young subjects. One possible reason for detecting such a large difference could be the passive protocol used by us as opposed to the active protocol adopted by the previous investigators cited above. It should be noted that when the brain issues a descending motor command signal to the limb muscles, corollary discharges are being sent simultaneously to relevant cortical areas, the so called “efferent copy” (11). In other words, the brain will receive corollary discharges from descending cortical signals, as well as ascending limb proprioceptive afferent inputs coding limb position and movement, when active as opposed to passive repositioning is employed. Hence, a passive joint repositioning test would produce greater angle errors than an active test. Also, the afferent input from the muscle spindles is relatively less in the passive repositioning test as the muscles are in a relaxed state (27). Consequently, subjects have to rely more on other sources of afferent inputs, such as those from the ligaments and joints, which are known to degenerate with aging (2). The amplitude of joint movement used in this study was only 3°, which was much smaller than that used in the studies cited above. It is possible that smaller changes in knee position might demand higher proprioceptive sensitivity for the knee joint to detect. Hence, the angle errors could have been larger than the case when larger changes in knee position were used. Please note that we had already shown that the passive knee repositioning test protocol adopted by us produced highly repeatable data in a previous study (24). This could be attributed to the well-controlled test parameters in our test protocol, which kept the initial joint position as well as the amount, speed and direction of joint movement constant. All these parameters are known to modulate the discharges of the joint proprioceptors (4). Hence, their proper control would be expected to ensure the accuracy of joint repositioning. This was supported by our finding of high data repeatability with an intraclass correlation coefficient of 0.90 in a previous study (24).
Limits of stability (LOS).
Studies have shown that the LOS can be used as a significant predictor of performance in functional activities, such as crossing a street, getting onto a bus and climbing a flight of 27 stairs (23). It also plays a significant role in indicating susceptibility to falls (5).
In the present study, the elderly control subjects showed a slower reaction time (by 100%), smaller maximum excursion (by 14%), and less directional control of their leaning trajectory (by 11%) than did the young subjects (all P < 0.05;Table 2). These declines in LOS performance of elderly subjects agreed with the findings from different studies using similar outcome measures. King et al. (10) found that the active older subjects (age range, 60–91 yr) had a decrease of 30% in the maximum forward and backward displacement of the COP normalized with respect to foot length, when compared with that of the younger subjects (age range, 20–59 yr). In another study, Hageman et al. (6) measured the total time moving from center to the eight target positions (termed as movement time), and the mean distance traveled from the center to each of eight target positions normalized with its respective shortest distance (termed as path length). They found that older adults (mean age = 65.3 yr) had longer movement time (by 49%) and path length (by 12%) when compared with those of the young adults (mean age = 25.3 yr).
Joint Proprioception Sense and Limits of Stability: Effects of Tai Chi Practice
Joint proprioception sense.
Our results showed that the male elderly Tai Chi practitioners achieved significantly smaller knee angle errors (mean = 1.7 ± 1.3°), when compared with those of the elderly control subjects (mean = 3.9 ± 3.1°; P < 0.05). Moreover, their performance was comparable to that of young subjects (mean = 1.1 ± 0.5°; P > 0.05;Table 2). In other words, experienced Tai Chi practitioners had developed a heightened sense of knee joint proprioception. Practicing Tai Chi involves doing a series of slow and precise movements, often repeatedly. The body and limb joints must be placed in specific positions relative to each other and in space (26). The subjects in our study had been practicing these slow and precise movements for 8.4 ± 9.1 yr (Table 1). It is thus entirely plausible that repeated Tai Chi practice could have improved their knee joint position sense.
We had previously proposed two mechanisms that could have given rise to the improvement of joint proprioception through long-term Tai Chi practice (24): 1) Plastic changes could have been induced in the cortex, by repeated positioning of body and limb joints in specific spatial positions as demanded by the various Tai Chi forms. 2) Increased output of the muscle spindles through the so-called γ route could have occurred during Tai Chi practice, which could help to bring about plastic changes in the central nervous system, such as an increased strength of synaptic connections and/or structural changes in the organization and numbers of connections among neurons (21).
Limits of stability (LOS).
Our results from the LOS test also showed that the male elderly Tai Chi practitioners achieved significantly faster reaction times (0.8 ± 0.1 s), as well as greater maximum excursions (92.6 ± 5.5%) and directional control of their normalized COP (79.0 ± 4.1%) than those of the elderly control subjects (1.0 ± 0.3 s, 83.2 ± 8.2%, 70.3 ± 7.3 s, respectively, P < 0.02;Table 2). The more superior performance of the Tai Chi practitioners in these three outcome measures revealed that repeated Tai Chi practice could have improved their dynamic balance control during self-initiated weight shifting within the subjects’ base of support.
Practicing Tai Chi requires shifting the body weight to different target positions in a smooth and coordinated manner. In other words, the subjects had regularly been challenging their balance control systems to maintain their center of mass within their base of support, when it was shifted to the limits of stability. It is hardly surprising that in our Tai Chi practitioners such a repetitive demand for proper balance control over a period of 8.4 ± 9.1 yr of practice could have developed better maximum excursion and directional control of their normalized COP than those of the control subjects. Indeed, the Tai Chi practitioners were found to be comparable to the young control subjects in these two measures, being respectively 92.6 ± 5.5%, 79.0 ± 4.1% in the former and 97.1 ± 3.3%, 79.2 ± 7.0% in the latter subjects (P > 0.05;Table 2). As the present findings are from a cross-sectional study, an argument naturally arises that these Tai Chi practitioners already had better balance control before they took up Tai Chi practice. To circumvent the possibility of sample bias, we had conducted a control trial with a prospective design (8). Elderly subjects (mean age = 67.6 yr) who underwent Tai Chi practice for 1.5 h, 6× wk−1 for 8 wk, had significantly improved the directional control of their normalized COP after 4 wk of training, whereas the control group receiving general education for a comparable period had no improvement in their balance performance.
The reaction time in initiating a movement depends on both neuromuscular control and cognitive factors (21). Lord and Fitzpatrick (13) measured the reaction time of a group of older subjects, aged from 62 to 95 yr, by instructing them to step on one of four targets with either leg as quickly as possible when it was illuminated. They found that leg muscle weakness, slow decision time as reflected by finger-press reaction time test, and poor leaning balance impaired the reaction time of their stepping on the illuminated target. Better balance control to stabilize the body in advance of potentially destabilizing movements (25), and further leaning distance and smoother control of leaning trajectory as shown in our present study, might explain why the elderly Tai Chi practitioners had shorter reaction times than those of the elderly control subjects, when shifting their weight to the eight target positions. Despite these improvements, we found that the reaction times of the elderly Tai Chi practitioners (mean = 0.8 ± 0.1 s) were still significantly slower than those of the young control subjects (mean = 0.5 ± 0.1 s, P < 0.05;Table 2). The finding of slower reaction times in the elderly subjects had also been demonstrated by Patla et al. (16). These investigators compared a group of healthy elderly subjects (mean age = 69 yr) with young subjects (mean age = 20 yr), by asking them to step in one of three directions, namely forward, sideways, and backward with the designated leg, after a light response signal. They found that the reaction time increased significantly in the elderly subjects. Further analysis using the vertical force component of forceplate revealed that elderly subjects took longer time to reach peak force in all three stepping directions, as well as lower peak force for forward stepping. The peak force was required to transfer body weight to the nonstepping leg.
Tai Chi exercise is regarded as a moderate form of exercise. Although its practice has been found to improve knee muscle strength in the older subjects (12), its training intensity on the leg muscle may not have produced sufficient increase in muscle strength, to help the elderly subjects to generate as fast a reaction time as that of the young subjects. Another contributing factor to the slower reaction time is the known decrease in conduction velocity in the elderly subjects. In this connection, using magnetic stimulation of the brain, Tobimatsu et al. (22) found that aging had a significant effect on prolonging the descending motor evoked potential latencies in the leg abductor hallucis muscles of the foot. In our study, the subjects had to recruit postural muscles including those of the lower legs to shift their weight to the target positions as fast as possible. The slower conduction velocity of the elderly subjects may thus explain in part or whole why the elderly Tai Chi practitioners still showed slower reaction times, when compared with those of young control subjects.
Joint proprioception sense and limits of stability: Comparison of Tai Chi practitioners versus golfers.
Our findings further demonstrated that the male elderly golfers achieved levels of knee joint proprioceptive acuity similar to those of the elderly Tai Chi practitioners, with absolute angle errors equal to 1.3 ± 0.7° and 1.7 ± 1.3°, respectively (P > 0.05;Table 2). In addition, the elderly golfers achieved a similar level of balance performance as the Tai Chi practitioners, in terms of reaction times (golfers = 0.8 ± 0.2 s; Tai Chi practitioners = 0.8 ± 0.1 s), maximum excursion (golfers = 92.9 ± 5.7%; Tai Chi practitioners = 92.6 ± 5.5%) and directional control of their normalized COP (golfers = 78.3 ± 5.4%; Tai Chi practitioners = 79.0 ± 4.1%) (all P > 0.05, Table 2). As with the Tai Chi practitioners, the elderly golfers achieved a performance level in the joint repositioning and LOS test comparable to that of the young subjects, except for the reaction time in the LOS test.
In a well-executed golf swing, golfers must maintain good balance and precise control of the posture of the head and body in relation to space and to the limb, as well as timely coordination of their muscle activities (19). As with Tai Chi, these requirements might explain the improved joint proprioception sense and balance control with repeated practice of golf over time. There has been a lack of research studies on the effect of golfing on joint proprioception and balance control. The present results thus add new and original knowledge to the benefits of golfing. Furthermore, our findings in both experienced Tai Chi practitioners and golfers suggest that exercise which demands accurate positioning of the body and limbs in space and in relation to each other is likely to improve joint proprioception sense. A similar line of thought may apply to the improvement in balance control found in these two groups of elderly subjects, in that both Tai Chi and golfing demand precise postural orientation of the head and body with respect to their limbs, as well as controlled weight shifting in single and/or double leg stand with various arm movements. In sum, the positive findings from our study provide potentially scientific support of the benefits of the two exercises, Tai Chi and golf, for the elderly subjects in the two functions that are known to decrease with aging, namely joint proprioception and balance control when subjects voluntarily shift weight within their base of support.
Correlation between knee joint position sense and LOS measures.
Subjects who had more acute knee proprioception responded more quickly in shifting their weight toward one of the eight target position, when it was lit up during the LOS test. This is clearly shown by the positive correlation between the absolute angle errors and the reaction times in moving the normalized COP during the test (r = 0.427, P = 0.013;Table 3;Fig. 1a), plotted with the data from all three elderly groups. This result further elaborated on the finding of Lord and Fitzpatrick (13), who showed that subjects with a history of falls had 13% longer reaction time than that of nonfallers (1.32 s and 1.17 s). Lord’s group measured the reaction time by asking the elderly subjects to step on one of four targets as quickly as possible when it was illuminated. The elderly Tai Chi practitioners and golfers in the present study had significantly shorter reaction times (0.8 s in both groups;Table 2), when compared with that of elderly control subjects (1.0 s, P < 0.05). Table 3 and Figure 1a further showed that improved knee joint proprioception, as shown by smaller angle errors in the passive knee repositioning test, was correlated with shorter reaction times in the LOS test. The finding of a faster reaction time in voluntary weight shifting helped to explain the report by Wolf et al. (29) of a reduced risk of multiple falls (by 47.5%) among elderly Tai Chi practitioners.
Our finding showed that the absolute angle error in the passive knee joint repositioning test was also inversely correlated with the maximum excursion in the LOS test (r = −0.522, P = 0.002;Table 3;Fig. 1b). In other words, subjects with more acute knee joint position sense had more extensive limits of stability. Previous studies have shown that the limits of stability decrease with age (6) and that this is a significant predictor of multiple falls (5). Our present finding may help to explain why Tai Chi practice has been shown to reduce the fear of falling and the risk of multiple falls among the elderly subjects (29).
Our results further demonstrated that the absolute angle of error in the passive knee joint repositioning test was inversely correlated with the directional control of the subject’s normalized COP in the LOS test (r = −0.396, P = 0.023;Table 3;Fig. 1c). In other words, elderly subjects who had better acuity of the knee joint position sense were able to maintain better directional control of their leaning trajectory to the specified target positions. The concept of directional control is based on the assumption that straight-line movements to the target positions are the most efficient and therefore better coordinated (15). Both Tai Chi and golfing require the practitioners to shift their body weight in a smooth and coordinated manner (19,26), which may enhance the directional control of their leaning trajectory. How the quality of directional control is related to daily activities has not yet been delineated, and further research is warranted in this area.
As aforementioned, the correlations between the absolute angle errors and the three LOS measures were statistically significant, with degrees of association ranged from −0.522 to 0.427 (all P < 0.05;Table 3). However, in one of our previous studies, we could not find any significant correlation between the absolute angle errors and the body sway in both anteroposterior and mediolateral directions, when 42 elderly subjects (mean age = 71 yr) stood quietly with feet together for 30 s with their eyes open (24). In this connection, Lord and colleagues (14) correlated the knee angle error in a limb matching test, with the mediolateral body sway in a near-tandem stability test with the eyes open, and found a statistically significant but low correlation (r = 0.19). Taken together, these findings suggest that knee joint proprioception is more important in the control of dynamic balance involving voluntary weight shifting than static standing balance. Though statistically significant, the correlation values were small. This finding could be attributed to the fact that postural control requires both sensory input (the information to detect the position and movement of the body in space) and motor output (the ability to generate forces for movement of the body) (21). Furthermore, the sensory input includes all the information from the somatosensory, visual and vestibular systems, and somatosensory information consists of proprioceptive inputs from the neck, body, and limbs (4). In other words, knee joint position sense is only one of the many sensory inputs that the brain can use for postural control. This would explain why there were only fair to moderate degrees of association between the knee joint position sense and LOS measures in the present study.
In conclusion, our study has provided evidence that male elderly subjects who had practiced Tai Chi or golf on average for more than 8 yr had better knee joint proprioception and greater limits of stability significantly beyond those of the control subjects similar in age, gender, and physical activity level. Of particular interest were the results showing that their knee joint proprioceptive acuity, as well as the maximum excursion and directional control of their normalized COP during weight shifting within their base of support, were even comparable to those of the young subjects. These findings suggest that long-term practice of Tai Chi and golf may improve joint proprioceptive acuity and dynamic standing balance control within the limits of stability in the elderly subjects, despite the known aging effects in these specific sensorimotor functions. The significant correlations found between the absolute angle errors in passive knee joint repositioning on the one hand, and the reaction time, maximum excursion, and directional control of the normalized COP in the LOS test on the other, highlight the importance of knee position sense in functional activities involving leaning or weight shifting. Nevertheless, because a cross-sectional design was employed in the present study, the findings should be confirmed in prospective intervention studies.
The authors thank the Hong Kong Polytechnic University for its financial support through an Area of Strategic Development Grant to C. W. Y. Hui-Chan and W. W. N. Tsang et al. We thank the subjects for their participation and the elderly centers for permission to recruit subjects.
No commercial party having a direct financial interest in the research findings reported here has, or will confer a benefit upon the authors or upon any organization with which the authors are associated.
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