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Direction-specific impairments of limits of stability in individuals with multiple sclerosis
Annals of Physical and Rehabilitation Medicine (Available online 8 May 2015)
Impaired postural control in individuals with multiple sclerosis (MS) is associated with falls. The objective was to evaluate the direction-specific limits of stability in people with MS.
Balance control of 18 individuals with relapsing-remitting MS and 18 healthy controls was assessed using instrumented (Limits of Stability (LOS) test) and clinical (Berg Balance Scale (BBS) and Activities-specific Balance Confidence (ABC) scale) tests.
There were significant differences in reaction time, movement velocity, endpoint excursion, maximum excursion, and directional control measures of the LOS test between individuals with MS and healthy controls. The BBS and ABC clinical balance measures were significantly lower in individuals with MS compared to control subjects. The directional control impairment was seen in the right side and backward diagonals (backward-right and backward-left) directions. A significant difference between the fallers and non-fallers was found on all the components of the LOS test. There was a significant correlation between the BBS and ABC scores and different components of the LOS test.
Direction-specific impairment of limits of stability components was observed in individuals with MS. This information could be used in balance rehabilitation of people with MS.
Keywords: Multiple sclerosis, Balance, Limits of stability, Dynamic posturography, Falls.
Balance impairment is frequently described as one of the early symptoms of multiple sclerosis (MS)  and  and approximately 75% of individuals with MS experience impairment of balance during the course of the disease  . Impairment in balance control could be seen in people with MS with significant clinical symptoms  , with minimal symptoms  and , and even with no clinical symptoms  . Balance impairment is a significant contributing factor for fall risk in people with MS  and  and is also often associated with mobility limitations and reduced engagement in physical activity  .
Quantifying the balance impairments is an essential part of monitoring the progression of the disease as well as assessing the therapeutic outcomes  . Clinical balance assessments such as the Berg Balance Scale  , Tinetti performance-oriented mobility assessment  , and Timed Up and Go Test  provide important information on balance deficits and fall risks in individuals with MS. However, studies have shown that the use of these assessment tools is limited by a ceiling effect and that these tests have limited value when trying to assess fall risks in active older adults  . It is also widely accepted that instrumented tests of balance allow obtaining more accurate measurements of subjects’ postural stability , , and . For example, assessment of postural stability using the limits of stability (LOS) is a valid and reliable outcome measure  .
It was reported in the literature that individuals with MS have reduced LOS scores as compared to healthy controls , , and . For example, individuals with MS showed deficiency in performance of the functional reach test, step test, and while responding to a brief backward tug  . It was also described in the literature that individuals with MS compared to healthy controls have significant balance deficits and poor balance confidence levels  . However, there is not enough information on the direction-specific balance impairment in individuals with MS. Hence, the aim of this study was to investigate the components of limits of stability in individuals with MS and compare their performance with that of healthy age and gender matched control subjects. We hypothesized that individuals with MS, as compared to healthy controls, will demonstrate impairment of limits of stability in the diagonal and backward directions.
2. Material and methods
Eighteen individuals with relapsing-remitting MS and eighteen age and gender matched healthy control subjects participated in the study ( Table 1 ). The inclusion criteria for individuals with MS were Expanded Disability Status Scale (EDSS) score of ≤ 4 (fully ambulatory, self-sufficient, and able to stand and walk without any aid or orthosis at least 500 meters), no relapse within the last three months, and normal or corrected to normal vision. All participants were right hand and leg dominant as confirmed by the Edinburg Inventory. Based on self-reports about experiencing falls during the previous 12 months, individuals with MS were categorized as either fallers (two or more than two falls) or non-fallers. The study was approved by the university's Institutional Review Board.
|Variables||MS (n = 18)||Controls (n = 18)||P-value|
|Age (years)||52.7 ± 12.2||50.0 ± 13.3||0.531|
|Height (cm)||166.6 ± 9.6||163.4 ± 8.0||0.292|
|Weight (kg)||70.1 ± 13.0||72.3 ± 11.1||0.590|
|BMI (kg/m2)||25.4 ± 5.5||27.0 ± 3.6||0.301|
|ABC score||70.28 ± 20.47||93.77 ± 6.25||< 0.001|
|BBS score||48.61 ± 6.73||55.17 ± 1.25||< 0.001|
|Gender ratio (male: female)||4:14||4:14||–|
|MS duration (years)||18.8 ± 9.4||–||–|
|EDSS score||2.69 ± 0.6||–||–|
MS: multiple sclerosis; EDSS: Expanded Disability Status Scale; ABC: Activity-specific Balance Confidence Scale; BBS: Berg Balance Scale; P-value for ABC and BBS refers to the Mann–Whitney U test. P-value for continuous variables, P-value refers to the independent sample t-test. Significant P-vaues are shown in bold.
Computerized dynamic posturography was used to perform the limits of stability test (EquiTest, NeuroCom, USA). The subjects were required to stand straight on the EquiTest platform keeping the cursor representing their body's center of gravity (COG) over the initial position shown on the computer monitor  . The subjects’ feet were aligned along the heel and medial malleolus landmarks printed on the top of the platform. The subjects were then instructed to shift their body weight (using their ankle joints as the primary axis of motion, without changing the feet position) in eight different directions (one direction at a time) as quickly as possible following the appearance of a target on the monitor. Each direction of the target was randomly selected by the researcher and displayed for eight seconds only once. The eight directions were: forward (FW), backward (BW), right (RT), left (LT), forward-right (FWRT), forward-left (FWLT), backward-right (BWRT), and backward-left (BWLT). For each direction the EquiTest software measured movement reaction time (ReT), movement velocity (MVL), endpoint excursion (EPE), maximum excursion (MXE), and movement directional control (DCL)  . The ReT in seconds reflects the onset of intentional movement toward the target as soon as the specific target appears on the screen. The MVL is the average speed of the center of gravity (COG) movement in degrees per second quantified for 5% to 95% of the distance from the center of the monitor (initial position) to the target. The EPE is the distance of the first movement toward the designated target, expressed as a percentage of maximum LOS distance. The endpoint is considered to be the point at which the initial movement toward the target ceases. The EPE is the excursion of the COG movement at first attempt in a particular direction: it provides a measure of how far the patient is willing to move on his first attempt shifting toward the target and reflects the participant's perception of his own safety limits  . The MXE refers to a maximum distance achieved during the trial: as such, the MXE is larger than the EPE. Both the EPE and MXE were calculated and expressed as a percentage of the maximum LOS distance (theoretical limits of stability). The theoretical LOS refers to the body leaning in ankle joints with angles of 8 degrees right-side, 8 degrees left-side, 8 degrees anteriorly, and 4.5 degrees posteriorly  . The measure of DCL is a comparison of the path of movement exhibited by the participant in the intended direction in which the values approaching 100% is a straight path i.e. toward the target, to the amount of extraneous movement away from the target, and is presented as a percentage (%). In addition, the composite score was calculated as an average score of the eight direction scores for each, ReT, MVL, EPE, MXE and DCL, and used to compare the groups of fallers and non-fallers.
Clinical balance measures included Berg Balance Scale (BBS) and Activities-specific Balance Confidence (ABC) scale.
The BBS is a valid  and reliable  tool to assess balance in individuals with MS. BBS contains 14 items where participants are rated on their ability to maintain positions or perform movements with increasing difficulty level and the ability to change positions  . Each item score ranges from 0 (unable to perform task) to 4 (normal). The maximum attainable score is 56.
The ABC scale is a valid and reliable scale of balance confidence used in individuals with MS  and ; it is correlated with the outcomes of the instrumented tests of balance. It contains a 16-item self-report questionnaire rating balance confidence in performance of various ambulatory activities without losing balance  .
2.3. Statistical analysis
A two way ANOVA was performed with the factors of group (MS and controls) and direction (8 directions) for each continuous variable (ReT, MVL, EPE, MXE, and DCL). Bonferonni correction was used for post-hoc comparisons. Mann–Whitney U test was used for the ordinal scale outcome measures EDSS, BBS and ABC scores and sub-group of fallers vs non-fallers. Spearman correlation coefficient (ρ) was used to evaluate the association between ABC scores, BBS scores, and the components of the LOS test. The statistical significance was set at P < 0.05. Fisher exact test was used for comparing the frequency of patient distribution with cerebellar insolvent between the groups.
The mean EDSS score for the MS group was 2.6 ± 0.6, which indicates mild level of disability. The mean duration of the disease was 18.8 ± 9.4 years. There was no significant difference in the age, height, and weight between the individuals with MS and healthy controls ( Table 1 ).
The center of gravity (COG) path recorded from a representative individual with MS and a healthy control subject during performance of the limits of stability (LOS) test is shown in Fig. 1 . Note a shorter COG path in most directions in the individual with MS. The mean values of LOS components for the MS group and the group of healthy controls are presented in Table 2 .
|Variables||Reaction time (ReT) (s)||Movement velocity (MVL) (deg/s)||Endpoint excursion (EPE) (%)||Maximal excursion (MXE) (%)||Directional control (DCL) (%)|
|Group effect||F = 5.86; P = 0.016||F = 30.80; P < 0.001||F = 43.39; P < 0.001||F = 32.346; P < 0.001||F = 30.69; P < 0.001|
|Directions||Groups||Mean ± SD||P-value||Mean ± SD||P-value||Mean ± SD||P-value||Mean ± SD||P-value||Mean ± SD||P-value|
|FW||MS||1.09 ± 0.6||0.215||2.68 ± 1.3||0.199||50.19 ± 22.3||0.048||73.88 ± 14.7||0.151||80.75 ± 9.2||0.114|
|Control||0.9 ± 0.34||3.46 ± 1.5||64.94 ± 22.5||81.50 ± 12.9||87.67 ± 5.7|
|FWRT||MS||1.05 ± 0.3||0.098||3.16 ± 1.1||0.005||69.69 ± 18.8||0.032||85.13 ± 10.6||0.093||73.38 ± 12.1||0.482|
|Control||0.80 ± 0.3||4.87 ± 2.7||85.72 ± 16.8||94.06 ± 12.9||76.44 ± 13.0|
|RT||MS||1.14 ± 0.5||0.037||3.49 ± 1.5||0.015||69.88 ± 23.7||0.028||83.38 ± 16.1||0.021||83.25 ± 5.3||0.188|
|Control||0.82 ± 0.34||4.97 ± 2.5||86.22 ± 14.5||95.67 ± 10.0||89.00 ± 4.6|
|BWRT||MS||1.00 ± 0.6||0.210||2.88 ± 0.9||0.029||54.25 ± 24.5||< 0.001||81.00 ± 22.0||0.002||62.51 ± 16.1||0.002|
|Control||0.81 ± 0.34||4.21 ± 2.4||83.33 ± 25.5||97.83 ± 15.8||76.06 ± 9.8|
|BW||MS||0.78 ± 0.2||0.849||2.54 ± 1.1||0.941||52.09 ± 11.0||0.499||69.45 ± 16.67||0.357||65.51 ± 15.4||0.021|
|Control||0.81 ± 0.5||2.59 ± 1.5||57.11 ± 19.1||74.33 ± 16.7||75.61 ± 12.7|
|BWLT||MS||0.80 ± 0.5||0.943||2.86 ± 0.9||0.048||55.94 ± 27.3||< 0.001||75.31 ± 20.4||< 0 .001||50.56 ± 23.9||< 0.001|
|Control||0.81 ± 0.5||4.06 ± 1.9||82.72 ± 24.3||93.67 ± 17.1||69.83 ± 12.8|
|LT||MS||0.99 ± 0.4||0.555||3.50 ± 1.4||0.007||67.38 ± 19.4||0.049||85.00 ± 15.6||0.069||80.75 ± 11.8||0.123|
|Control||0.89 ± 0.4||5.16 ± 2.1||82.06 ± 26.7||94.67 ± 9.3||87.50 ± 4.3|
|FWLT||MS||0.89 ± 0.6||0.797||3.33 ± 1.1||0.034||72.71 ± 26.2||0.037||89.31 ± 17.5||0.219||75.13 ± 15.6||0.510|
|Control||0.85 ± 0.4||4.62 ± 2.1||88.22 ± 15.2||95.83 ± 13.5||78.00 ± 15.9|
FW: forward; FWRT: forward-right; RT-right; BWRT: backward-right; BW: backward; BWLT: backward-left; LT: left; FWLT: forward-left; MS: multiple sclerosis; bold values are significant P-values. Two individuals with MS could not complete the LOS test.
3.1. Reaction time and movement velocity
Significant group effects were observed for the reaction time (ReT) (F = 5.86, P = 0.016) and movement velocity (MVL) (F = 30.80, P < 0.001) measures. Post-hoc comparisons showed that for movement toward the right direction, reaction time was significantly longer in individuals with MS as compared to controls. At the same time, the movement velocity in individuals with MS was significantly lower in all the directions compared to controls except for in FW and BW directions.
A significant group effect was seen for the endpoint excursion (EPE) (F = 43.39; P < 0.001) and maximum excursion (MXE) (F = 32.34, P < 0.001) measures. Post-hoc analysis showed that EPE was significantly reduced in the MS group for all the directions except for the backward direction and MXE was significantly reduced for the RT, BWRT and BWLT directions.
3.3. Directional control
A significant group effect (F = 30.69, P < 0.001) was observed for the directional control (DCL) measure. Post-hoc comparisons demonstrated that the directional control was significantly reduced for the MS group in the BWRT, BWLT and BW directions.
3.4. Direction-specific impairments in limits of stability in individuals with MS
Fig. 2 illustrates the direction-specific impairments in individuals with MS on the LOS test. Thus, in the MS group as compared to the healthy controls, three directions, namely, RT, BWRT, and BWLT showed significant impairments in four out of five components of the LOS test. Thereafter, significant impairment was seen for FWRT, FWLT, and LT directions in two out of five components of the LOS test. The FW and BW directions were less affected with only one out of five components of the LOS test showing significant impairment.
3.5. BBS and ABC scale
Individuals with MS showed a significant reduction in the outcomes of the clinical balance measures using BBS (U = 40.00, P < 0.001) and ABC scores (U = 40.00, P < 0.001) as compared to healthy controls ( Table 1 ).
3.6. Correlation of clinical tests with components of the LOS test
There was a significant negative correlation between the BBS and ReT measures (ρ = –0.363; P = 0.035). There was also a positive correlation between the BBS and EPE (ρ = 0.507; P = 0.002), MXE (ρ = 0.503; P = 0.002) measures, and ABC (ρ = 0.509; P = 0.002) scores. The ABC scores showed a significant positive correlation with the EPE (ρ = 0.371; P = 0.031) and DCL (ρ = 0.348; P = 0.044) measures.
3.7. Fallers vs non-fallers
The composite scores for ReT, MVL, EPE, MXE, and DCL in the group of fallers were significantly lower than in the non-fallers group of individuals with MS. Moreover, fallers had significantly lower values for the BBS score (U = 14.00, P = 0.021) than non-fallers. However, no significant difference was observed for the ABC scores (which reflects a person's subjective balance confidence) between the fallers and non-fallers (U = 23.00, P = 0.131). The mean values, percentage differences in mean values for LOS, BBS, and ABC, and the comparisons between the fallers and non-fallers are reported in Table 3 .
|Variables||Non-fallers (n = 10)||Fallers (n = 8)||Percentage difference in mean value||P-value|
|LOS composite scores|
|ReT||1.50 ± 0.3||0.90 ± 0.2||66.67||0.002|
|MVL||3.30 ± 1.1||1.90 ± 0.6||42.43||0.011|
|EPE||66.00 ± 9.9||52.70 ± 6.8||20.16||0.007|
|MXE||80.60 ± 11.1||69.70 ± 4.6||13.53||0.022|
|DCL||70.56 ± 10.2||58.50 ± 8.3||17.17||0.022|
|EDSS||2.60 ± 0.6||2.81 ± 0.7||–||0.515|
|Patients with cerebellar signs||4||5||–||0.63|
|ABC score||76.50 ± 19.1||62.50 ± 20.6||18.21||0.146|
|BBS score||51.70 ± 4.9||44.80 ± 6.9||13.35||0.021|
ReT-reaction time; MVL: movement velocity; EPE: endpoint excursion; MXE: maximal excursion; DCL: directional control; EDSS: Expanded Disability Status Scale; ABC: Activity-specific Balance Confidence Scale; BBS: Berg Balance Scale; Significant P-values are shown in bold. Fisher's exact test was used for the analysis of the frequency distribution of patients with cerebellar involvement. Two subjects in the group of fallers could not complete the LOS task.
The inability to voluntarily shift the body toward limits of stability can contribute to instability during activities of daily living such as reaching for objects  and  and walking  . The available literature on the impairments of the limits of stability in individuals with MS is not complete because most of the studies provide information only on the disease-related impairments of limits of stability in anterior-posterior and medio-lateral directions , , , and .
For the first time, the outcome of the current study provides experimental data on the existence of a significant impairment in the limits of stability in individuals with MS in directions other than the four main directions described in the literature. Thus, the study participants with MS showed significant impairments in controlling the body shift in the diagonal and backward directions (RT, BWRT and BWLT diagonals). It is also important to mention that despite all individuals with MS having low levels of disability on the EDSS scale, their ability to control posture while leaning in the backward and diagonal directions and toward the right side was impaired. This suggests that the LOS test could be used to document the signs of balance impairment in individuals with MS during early stages of the disease progression.
4.1. Direction-specific limits of stability
Individuals with MS had impaired postural control primarily while shifting their body weight toward the RT, BWRT and BWLT directions confirmed by significantly diminished scores in four out of five components of the LOS test. These findings suggest that individuals with MS had impaired postural control on the right side and in the backward diagonal directions. The DCL scores in the MS group were significantly diminished for the BW, BWRT, and BWLT directions. Moreover, since the EPE excursion is the first attempt of the COG movement in a particular direction (which is usually smaller than the MXE that refers to the maximum voluntary sway), the decreased EPE magnitudes seen in MS suggest that people with MS might have a false perception of their safety limits especially in the backward directions. Such a decreased EPE magnitude might reflect that individuals with MS have difficulties in controlling body inertia. This might explain why individuals with MS have limited excursion at a first attempt. Thus, the impairment of directional control combined with the false perception of their safety limits may make individuals with MS more at risk to trigger a balance reaction earlier in case of backward leaning, and when there are potential backward perturbations. Such vulnerability is exacerbated by the observation of slow movement velocity and decreased movement excursion toward the target in backward diagonals (BWRT and BWLT). These findings therefore suggest that there is a need to pay special attention to restoring the ability of individuals with MS to lean in the backward and diagonal directions during balance rehabilitation.
In this study, the overall performance on the LOS test by individuals with MS (schematically shown in Fig. 2 ) was significantly impaired as compared to that of the control subjects. There are noticeable clusters of deterioration of balance control in individuals with MS confirmed by the results of the LOS test. For example, one cluster includes impairments of directional control (DCL), movement velocity (MVL), maximum excursion (MXE), and endpoint excursion (EPE) in the BWLT, BWRT and RT directions. It appears that individuals with MS experienced greater challenges performing the task in the backward left and backward right directions. At the same time, the performance of the individuals with MS in the BW direction did not differ from controls which could be explained by a decreased confidence of both groups while shifting the body weight in the BW direction.
When performing the task, the study participants relied on visual cues (indicating the direction the participants were required to lean their body) that were displayed on the monitor located in front of the subjects. It looks like individuals with MS had some difficulties in translating information about the position of the target into the execution of body movements in a BWLT and BWRT diagonals. Additional studies are needed to investigate this issue further. On the other hand, healthy individuals were able to better utilize available visual information for postural control. This outcome is in line with the literature on the age-related decline of the limits of stability seen mainly in the leftward and rightward directions  .
4.2. Role of history of falls
The group of fallers demonstrated significantly reduced magnitudes of all the components of the LOS test as compared to the non-fallers ( Table 3 ). Thus, the group of individuals with MS who experienced falls had significantly reduced ReT, MVL, EPE, MXE and DCL compared to non-fallers. Since the EDSS scores of both the groups were comparable and the distribution of patients with cerebellar involvement was not significantly different between the groups (P = 0.63), one could conclude that the dynamic posturography test is sensitive enough to identify the fallers among individuals with MS with low level of disability. Nevertheless, the mean reaction time in fallers was 66.67% reduced and the mean movement velocity was 42.43% reduced as compared to non-fallers. It is reported in the literature that longer reaction time could describe defective sensory motor integration in preparing the task in MS  . Moreover, a shorter reaction time represents a better clinical outcome and a prolonged reaction time is associated with the negative effect of the task demands in MS  . While the outcome of the analysis on ReT between individuals with MS and controls is in agreement with previous reports, the results of analysis of groups of fallers and non-fallers are in contrast with the results of clinical outcome, possibly indicating that reduced ReT in the group of fallers could be due to methodological reasons. As such, this outcome could exemplify a possible limitation of using the ReT to distinguish between the fallers and non-fallers. On the other hand, smaller MVL, EPE, MXE and DCL measures were associated with decreased balance capacities and as such could be used to distinguish between fallers and non-fallers.
At the same time, the reduced movement velocity recorded in the group of fallers in the present study could be an indication that these individuals are more cautious (thus slower) while performing activities that can potentially endanger their balance. This outcome suggests that prior exposure to falls in individuals with MS is translated into slower performance of the entire movement or a task. However, it looks like experiencing falls is not translated into slower initiation of the movement. This result highlights the need for individuals with MS to perform tasks involving balance maintenance slower and/or to use fall prevention strategies such as turning lights on when moving around the home and asking for help with some activities  .
Significantly lower values of BBS scores were also recorded in fallers compared to non-fallers. The BBS outcome taken together with the diminished performance on the LOS test suggests that individuals with MS with a history of falls indeed have greater balance impairment confirmed by the objective instrumented and clinical tests.
However, the ABC scores that characterize self-reported balance confidence (and as such subjective) were not significantly different between the fallers and non-fallers. In contrast to our results, significant differences in the confidence levels were reported in the literature between the fallers and non-fallers  and . The dissimilarity in the confidence levels between the former and current studies could be explained by the differences in the level of disability of the study participants. Thus, individuals with the EDSS score of ≤ 4 were included in the current study, while the participants in the cited studies had a wider range of disabilities (EDSS ≥ 6.0). Nevertheless, the outcome of the current study suggests that individuals with MS, especially those with mild impairments, may overestimate their ability to handle daily tasks involving balance maintenance.
Individuals with MS as a group clinically demonstrated impaired balance reflected by significantly lower BBS and ABC scale scores as compared to healthy controls. These results are in line with previous findings  and . Moreover, a significant correlation of different components of the LOS test with ABC and BBS tests suggests that both the clinical scales and instrumented measures provide reliable information and could be used to assess balance in individuals with MS.
It is important to note that the results of this study indicate that postural stability assessed using the LOS test is compromised in people with MS despite low clinical disability. This outcome taken together with the literature data on gait and balance problems in individuals with MS in the absence of disability  and  suggests the potentials of using instrumented tests in balance rehabilitation of individuals with MS.
Individuals with MS have direction-specific balance impairment, more prevalent in right and backward diagonal directions. The LOS test could be used to identify minimal postural impairment in people with MS and differentiate between fallers and non-fallers. The LOS test measures can be used in balance rehabilitation of people with MS.
Disclosure of interest
The authors declare that they have no conflicts of interest concerning this article.
We thank the individuals with MS and control subjects for their exceptional cooperation. This work was partially supported by the National Multiple Sclerosis Society grant # MB 0023.
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Department of Physical Therapy, University of Illinois, 1919, W.-Taylor street, 60612 Chicago, IL, USA
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