Background
Vestibulopathy decreases whole body dynamic postural control and causes functional limitations [
1‐
4]. Limitations in ambulation, dynamic balance and trunk control, for example, can lead to disability and contribute to decreased quality of life [
5]. Vestibular rehabilitation (VR) is a well-accepted exercise program intended to remedy balance impairment caused by damage to the peripheral vestibular system [
6]. Vestibulopathy impairs both the vestibulo-ocular reflex (VOR) and the vestibulo-spinal reflexes (VSR) [
7]; hence, VR is designed to adapt the CNS to diminished vestibular input and to compensate for VOR and VSR loss, via gaze and balance retraining, which in turn should improve whole body dynamic stability [
8‐
10].
Alternative therapies, such as Tai Chi (TC), have recently gained popularity as a treatment paradigm for a variety of human ailments, including balance impairment [
11‐
13]. TC employs detailed regimens of physical movement, breathing techniques, and cognitive tools to strengthen the body, relax the mind, and balance the flow of life force [
14]. The purported improvements in overall body control and mind-body focus with TC may offer an improved approach to treating balance dysfunction [
11,
13,
15‐
17]. Where the explicit objective of many VR exercises is to improve gaze stability, TC emphasizes a 'soft' unfocussed gaze during the prescribed balance exercises. Although there is strong evidence that VR [
4,
8‐
10,
18], and more recently TC [
11,
13,
15‐
17], can benefit people with vestibulopathy, the degree to which gait improvements may be related to neuromuscular adaptations of the lower extremities are unknown. Thus, although the end result of both TC and VR should be improved dynamic stability during locomotor activities of daily living, including gait, we hypothesized that the
mechanisms underlying such improvements should differ substantially. A better understanding of how balance dysfunction interventions affect lower extremity neuromuscular function during ADL may be useful for developing gait training exercises, and for providing a fuller understanding of the link between motor function and balance.
In this report, we present preliminary data from a blinded randomized clinical trial comparing the effects of VR and TC on gait function, joint kinetics and trunk kinematics in older adults. While the overall aim of this study was to determine the effects of balance rehabilitation on gait characteristics, we directed our efforts in this paper to better understand the relationship between mechanical energy transfers along the lower extremity kinematic chain (ankle-knee-hip), and forward and side-to-side velocity of the trunk.
Our general hypothesis was that adults with balance impairment from vestibulopathy who receive the VR or TC intervention will improve gait function as indicated by time-distance measures. Our specific hypotheses are based on the following rationale: Recent studies in healthy older adults [
19‐
21], with general impairments such as strength loss [
22], or pathologies such as knee arthritis [
23,
24], show that the hip musculature often aids, or compensates for, ankle plantar-flexor muscles in providing both forward propulsion and trunk stability [
25]. These prior studies have shown a consistent decline in plantar-flexor muscle power during gait, with an increase in hip muscle power, in older adults with, and without, known mobility impairments. As shown recently by Neptune and colleagues [
26], the ankle plantar flexors contribute significantly to both forward propulsion and vertical trunk stability. Thus, one would expect that improvements in lower extremity motor control, aimed at increasing forward propulsion and trunk stabilization, would be represented by decreases in hip mechanical energy expenditures and increases in ankle (and perhaps knee) mechanical energy expenditures, and be directly related to improved kinematics of the trunk.
Based on the above rationale, and the specific treatment programs described in the following sections, we hypothesized: 1) TC treatment will improve lower extremity motor control by increasing ankle mechanical energy expenditure (MEE) contribution, and decreasing hip MEE contributions, to total energy of the leg, more than VR; and 2) that improved trunk control following TC will be positively correlated with improvements in lower extremity motor control, while improvements in trunk control following VR will not be correlated with improvements in lower extremity motor control. The latter may indirectly implicate other mechanisms, most likely improvements in VOR/gaze stability [
27].
Discussion and conclusions
Little is known about the mechanisms of improved balance and postural control following rehabilitation in people with vestibulopathy. Although VR has shown promise for improving patients balance and gaze stability [
4,
9,
10,
29,
36‐
40], just over 65% of people treated respond to the therapy [
10]. Improvements in function are not ubiquitous with VR treatment. Alternative therapies, such as TC, offer a complementary approach to improving balance and postural control by teaching body control and awareness [
12,
15]. The purpose of the present study was to examine lower extremity neuromuscular function during gait in patients receiving either VR or TC treatment, and to examine how changes in neuromuscular patterns relate to changes in trunk control. Our first hypothesis, that patients receiving TC treatment will improve lower extremity motor control by increasing ankle MEE contribution and decreasing hip MEE contribution more so than the VR patients was not supported by analysis of between-group differences. However, in examining the within-groups changes (pre versus post-intervention), some potentially important biomechanical observations were made. Our second hypothesis, that trunk control in patients receiving TC will be positively correlated with improvements in lower extremity motor control, but trunk control in those receiving VR will not be positively correlated with improvements in lower extremity motor control, was supported.
Although an overall improvement in gait function (as indicated by time-distance measures) for both treatment groups was observed, confirming our general hypothesis, our data suggest that the mechanisms underlying those improvements differ, and appear to be linked to differences in neuromuscular responses of the lower extremities to the treatment programs. Specifically, our data suggest that changes in the relative contribution of individual joints to total leg mechanical energy expenditure (MEE), and the relationship between changes in lower extremity mechanical energy expenditure and changes in upper body kinematics, are different between TC and VR interventions (Figure
4). Further, these data highlight the importance of assessing gait not only with time-distance functional gait measures (Table
1), but also with measures that assess neuromuscular function of the lower extremities and control of the body's most massive segment, the trunk.
We found that TC patients significantly increased the contribution of ankle MEE to total leg MEE and decreased contribution of hip MEE to total leg MEE following the treatment program, while the VR group showed no significant change in ankle or hip MEE contributions following intervention (Figure
2). Although the changes were not statistically different between groups, the within groups comparisons suggest that clinically important trends may nonetheless be present in terms of biomechanical responses to the different therapies. Figure
1 shows the total joint MEE
(t) (sum of all transfer components) for ankle, knee and hip, and total leg MEE
(t), for each group. The increases in leg MEE
(t), which were similar for both groups, were apparently achieved by different neuromuscular adaptations of the individual joints. Where the VR group appear to increase total MEE
(t) of each joint to gain a total MEE increase of the leg, the TC group show a distinctive pattern of substituting ankle plantar-flexor contribution for hip extensor/flexor contribution. Prior studies on the relative roles of ankle and hip kinetics in gait [
19,
20,
24] suggest that the result observed for TC patients indicates a trend toward a reduction in hip compensation and increased use of ankle muscles to provide both propulsion and stability.
Figure
2 shows the percent contribution of the changes to the concentric leg MEE
(+) for the changes in concentric MEE
(+) of individual joints. While both groups decreased the relative contribution of concentric hip MEE
(+), only the TC group increased the contribution of ankle concentric MEE
(+), while the VR group increased the contribution of knee concentric MEE
(+). Concentric energy transfer represents the energy expended by muscles in concentric contraction when energy is being transferred between segments. Because concentric contraction represents work being done
by the muscles (as opposed to eccentric contraction, which is work being done
on the muscles), we can interpret the above finding as meaning that, for the TC group, a greater proportion in the change in concentric work done by the leg muscles is attributed to the change in concentric work of ankle plantar-dorsiflexors, while for the VR group, this contribution decreases.
One possible reason concentric ankle MEE contribution may have increased significantly in the TC group, but not the VR group, is because the TC and the warm-up exercises improved ankle flexibility. Tight ankles (limited range of motion, ROM) may preclude the optimal structural alignment to coordinate mechanical energy sufficiently to increase propulsion [
41], perhaps at the expense of trunk stabilization. Ankle function is important for balance corrections in both healthy elderly and vestibulopathic subjects [
42‐
44]. A study by Van Deusen et al. [
45] found that Tai Chi-like exercises for elders with arthritis resulted in a significant increase in ankle plantar flexion; this finding supports the above contention that the TC group in our study may have increased ankle MEE contribution as a result of increased ankle ROM, ankle moment, or both. The tight coupling between ankle and hip power in gait [
19] would also explain the neuromuscular adaptive decrease in hip MEE contribution. Given the importance of ankle-plantar flexors in both propulsion and trunk stability, we conclude that TC teaches optimization of MEE in an effort to control the trunk while improving lower extremity function. The relationship between lower extremity MEE and trunk kinematics for the two treatment groups lends further credibility to this conclusion.
As shown in Figure
4, the relationship between change in leg MEE and change in the range of forward trunk velocity was positive for the TC group, and negative for the VR group. Similar relationships were also observed between change in leg MEE and change in peak forward trunk velocity. The observed direct relationship for the TC group suggests that the redistribution of power among ankle, knee and hip joints, which resulted in a net increase in the total MEE of the leg, enabled these patients to attain a faster gait. This observation is expected based on the principles of TC, which emphasize a vertical alignment integrating the head, torso, hips and legs. This concept of integrated alignment is reflected in phrases from the TC classics such as ". suspend the spine like a necklace of pearls" and "movements are initiated in the feet, steered by the waist and administered through the hands." [
46]. In contrast, for the VR group, however, the increase in leg MEE was associated with a decrease in both peak and range of trunk velocity. This finding suggests that VR subjects, when increasing power generation/absorption with their lower extremities, reduce trunk oscillations during gait, possibly as a way to stabilize the trunk and head. This corrective procedure may not be necessary for TC subjects as they learned to move the trunk more proportionately to total lower extremity MEE, without need to explicitly attend to additional factors or mechanisms to stabilize the head. Although speculative, these scenarios correspond with the observed high positive correlation between change in leg MEE and change in trunk velocity peak and range seen after TC training but not after VR rehabilitation.
Because the VR exercise program may increase subjects' awareness of eye and head movement strategies that cause dizziness and instability [
8,
47], a more rigid head and trunk strategy during dynamic activities such as gait would be expected. The VR program's balance retraining exercises do not emphasize dynamic whole body movement patterns that improve overall postural control [
10]. Subjects practice maintaining balance in challenging postures (narrow base of support such as feet together and one-legged standing still) using a variety of self selected movement patterns. It is probable that subjects would make the trunk more rigid to lessen head movement during these tasks. The VR group's decrease in trunk velocity range with increase in mechanical energy of the lower extremities during gait appears to support this explanation. Within the TC group, the subjects practice series of movement patterns that include elements of controlled trunk rotation without instruction on eye fixation. The training of smoothly transitioning body segment motions may provide these subjects a different mode of compensation for their instability. Practice of the TC movements may promote more natural trunk movements similar to healthy persons as shown in our biomechanical findings during gait.
Although the preliminary results presented here suggest the lower extremities may play an important role in the ability of vestibulopathic patients to improve gait function, several limitations of the present study may prevent broad generalization of the results. Our small sample size was perhaps the most important limitation. It is probable that the lack of between-group significant changes, particularly in light of many significant within group differences (pre-post intervention), was due to high variances obscuring group mean differences. Indeed, a larger sample size for controlling type II errors (increasing power), and better control of type I errors for multiple statistical tests, is warranted for future full-scale studies. The large age range within groups may have also contributed to high variability, but note that more heterogeneous samples in fact enhance external validity, including generalizability, of the results. We also did not include a no-treatment control group in the experimental design of this preliminary study. Because vestibulopathic patients may learn to compensate spontaneously, a no-treatment or sham-treatment group would be necessary to determine if changes in gait function are truly a result of the interventions. This is unlikely, however, given the inclusion criteria that all subjects must have had stable symptoms for 6 months and were on average 3 year post-onset of vestibulopathy. Given that both groups improved gait function in our randomized design comparing substantially different interventions suggests that the effects observed were not spurious. It must be recognized, however, that assumed improvements in function, via increased gait speed for example, may be limited [
48,
49]. As well, we only analyzed the mechanics of the lower extremities in the sagittal plane. It is highly likely that compensations for lower limb power impairments occurred in frontal and transverse planes as well. Also, the different number of patients in each group having a diagnosis of UVH and BVH is a potential limitation. Although there were no significant differences in proportion of UVH and BVH between the two treatment groups, that the BVH patients were much more disabled than the UVH patients in this study may be important, even when the difference in proportions of diagnostic categories (BVH or UVH) within treatment groups is small. Lastly, although there were no significant differences in age and gender distribution between treatment groups, a larger study sample would allow such subgroup effects to be studied.
We conclude that VR and TC can successfully improve gait function, as determined by common time-distance measures, in patients with vestibulopathy. We further conclude, however, that TC improves lower extremity motor control more than VR, by selective redistribution of joint energetics, which appears to engender a more vigorous gait and better trunk control. TC, as a complementary treatment to VR, may allow for better control of the trunk through reorganization of lower-extremity motor patterns, elicited from the flowing, controlled TC exercises.
Competing interests
The author(s) declare that they have no competing interests.
Authors' contributions
All authors participated in the overall study design, contributed to the interpretation of data and writing/editing of the manuscript, and have read and approved the final manuscript. CAM conceived the hypotheses for this manuscript and carried out the data analysis; DEK was the principal investigator of the project; SWP was the neurologist associated with the project; DMS conducted the patient testing and assisted in development of the vestibular rehabilitation program; PMW conducted the Tai Chi intervention; and SLW was the project consultant.