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Gait Asymmetry in Community-Ambulating Stroke Survivors
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ORIGINAL ARTICLE
Gait Asymmetry in Community-Ambulating Stroke Survivors Kara K. Patterson, MSc, Iwona Parafianowicz, Cynthia J. Danells, MSc, Valerie Closson, MSc, Mary C. Verrier, MHSc, W. Richard Staines, PhD, Sandra E. Black, MD, PhD, William E. McIlroy, PhD ABSTRACT. Patterson KK, Parafianowicz I, Danells CJ, Closson V, Verrier MC, Staines WR, Black SE, McIlroy WE. Gait asymmetry in community-ambulating stroke survivors. Arch Phys Med Rehabil 2008;89:304-10. Objectives: To determine the prevalence and severity of asymmetry among independently ambulating stroke survivors and to establish the association between velocity and asymmetry. Design: Descriptive analysis. Setting: Research gait laboratory in a Canadian hospital. Participants: Community-dwelling, independently ambulating participants (N⫽54) with chronic stroke. Interventions: Not applicable. Main Outcome Measures: Overground gait velocity, symmetry ratios for temporal and spatial step parameters, and motor impairment of the foot and leg. Spatiotemporal parameters were collected with a pressure-sensitive mat. Motor impairment was measured clinically with the Chedoke-McMaster Stroke Assessment. Results: Thirty (55.5%) participants showed statistically significant temporal asymmetry and 18 (33.3%) exhibited statistically significant spatial asymmetry. Preferred velocity was negatively associated with temporal asymmetry (r⫽ ⫺.583, df⫽52, P⬍.001) but not spatial asymmetry (r⫽⫺.146, df⫽52, P⫽.29). Temporal asymmetry was also associated with motor recovery of the leg (r⫽ ⫺.644, df⫽35, P⬍.001) and foot (r⫽ ⫺.628, df⫽35, P⬍.001). Conclusions: The results of the current study illustrate that temporal asymmetry can be found in many independently ambulating stroke patients. The work highlights the need for a standard assessment of poststroke gait symmetry in light of the complex relationship with motor impairment and velocity. Key Words: Cerebrovascular accident; Gait disorders, neurologic; Rehabilitation. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
From the Heart and Stroke Foundation Centre for Stroke Recovery, Sunnybrook Health Sciences Centre, Toronto, ON, Canada (Patterson, Parafianowicz, Danells, Closson, Staines, Black, McIlroy); Toronto Rehabilitation Institute, Toronto, ON, Canada (Patterson, Verrier, Staines, McIlroy); Graduate Department of Rehabilitation Science, University of Toronto, Toronto, ON, Canada (Patterson, Verrier, Black, McIlroy); Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada (Staines, McIlroy); and Department of Physical Therapy, University of Toronto, Toronto, ON, Canada (Verrier). Supported by the Toronto Rehabilitation Institute, Marguerite Harland Smith Bursary, Lois Snelling Bursary, and the Canadian Institutes of Health Research (grant no. MOP62957). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to William E. McIlroy, PhD, Faculty of Applied Health Sciences, University of Waterloo, 200 University Ave W, Waterloo, ON N2L 3G1, Canada, e-mail: [email protected]. 0003-9993/08/8902-00318$34.00/0 doi:10.1016/j.apmr.2007.08.142
Arch Phys Med Rehabil Vol 89, February 2008
TROKE IS THE LEADING CAUSE of adult neurologic S disability affecting all aspects of life including mobility, activities of daily living, communication, and cognition. Gait deficits greatly contribute to functional disability after stroke, and of all stroke-related impairments, improvement of walking function is the goal most often stated by stroke patients.1 In light of the importance of gait, considerable attention has been focused on the measurement and improvement of gait velocity in persons with stroke.2-4 As a clinical measure, velocity reflects overall gait performance; however, it is limited in both its value to document poststroke recovery and the information it provides regarding the underlying impairments.5,6 In addition, gait velocity does not fully reflect all aspects of a typical stroke rehabilitation program and thus is limited as a solitary clinical measure to direct treatment and to reflect its outcomes. For example, in addition to increasing gait speed, considerable focus is placed on the equalization of weight bearing through the lower extremities and the capacity to shift weight between the lower extremities during gait.7,8 A complementary measure that may better reflect this particular aspect of rehabilitation is gait symmetry. Brandstater et al9 suggested that symmetry may characterize poststroke gait better than unilateral values. Normative gait tends to be symmetric both spatially (between left and right joint angles, step and stride lengths) and temporally (between right and left swing, stance, step and stride times), with interlimb differences in vertical force and temporal parameters less than 6%.7 In contrast, the unilateral deficits that occur after stroke are likely to result in gait asymmetry. Such asymmetry has been shown by measurement of limb-specific differences in kinematic and kinetic measures of gait as well as differences in overall spatiotemporal characteristics such as swing and stance times.10,11 Studies examining the symmetry of spatiotemporal parameters have described a gait pattern associated with a favoring of the paretic limb.10 That is, compared with the nonparetic lower extremity, swing phase duration is prolonged and single-limb support time is shortened on the paretic limb.9,10 A specific interest in the present study was the relationship between these 2 important aspects of gait recovery: symmetry and velocity. There have only been 2 studies that have specifically explored this relationship, and in both cases the studies primarily focused on temporal measures of gait for the index of symmetry.9,12 Unfortunately, the results from these studies are conflicting about the relationship between specific measures of gait symmetry and walking velocity. Roth et al12 found that while temporal gait components (swing symmetry and swing/ stance ratio in the paretic limb) were linearly correlated with walking velocity, overall temporal symmetry (paretic swing and/or paretic stance:nonparetic swing and/or nonparetic stance) was not related to velocity. On the other hand, Brandstater9 found that overall temporal symmetry was related to velocity. There is concern that the conflicting results of these studies may be attributed to relatively small sample sizes (⬍25 subjects). These studies may also be limited by the possibility that some subjects were permitted the use of canes, which may have had a profound impact on the symmetry-velocity relationship in some people.
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It is our view that gait velocity and temporal asymmetry are related, given that both features of poststroke gait correlate with the same impairment measures. Both gait velocity and temporal asymmetry have been shown to correlate with motor recovery, lower-extremity muscle strength, peak torque, total work, and spasticity, albeit to varying degrees.8,9,13 It may be that poor temporal symmetry may be a primary determinant of a slow gait velocity because of the associated challenges linked to asymmetry (eg, asymmetric limb loading, inefficiency, challenged balance control). Regardless of the nature of its relationship to velocity, asymmetry is an important issue to address in the rehabilitation of poststroke gait for several possible reasons including efficiency, overall activity level, and musculoskeletal health. It is believed that gait symmetry and energy expenditure are related and that symmetric gait is the most efficient pattern.14,15 People poststroke have higher energy expenditure during gait and extremely low ambulatory activity levels compared with healthy controls.16,17 It is possible that the asymmetric pattern of poststroke gait contributes to the observed increased energy expenditure. It is also possible that asymmetric chronic stroke patients reduce their overall activity levels over time in response to the increased cost of this gait pattern. Asymmetric poststroke gait may also negatively affect the musculoskeletal health of the nonparetic limb. High forces repetitively applied to a limb can lead to pain and joint degeneration.18,19 In stroke survivors, temporal asymmetry positively correlates with increased vertical ground reaction forces through the nonparetic lower limb.7 Therefore, over time, the asymmetric gait of a stroke patient exposes the nonparetic limb to increased repetitive loading. To our knowledge, there are no studies that have examined the incidence of joint pain and degeneration in the stroke population. However, a few studies of the amputee population have reported an increased incidence of joint pain and degeneration and an increased risk for osteoarthritis in the intact limb of amputees.18,19 These musculoskeletal issues identified in the amputee population have been attributed to greater ground reaction forces through the intact limb compared with the amputated limb, associated with gait asymmetry.18,19 It seems reasonable to assume that the same asymmetric pattern seen in the stroke population could lead to the same musculoskeletal consequences in the nonparetic limb. In light of the potential long-term implications of persisting gait asymmetry (decreased efficiency, decreased activity level, musculoskeletal injury) and its possible use as an objective clinical gait measure, there is a need to better understand the occurrence and severity of asymmetry among ambulating stroke survivors. It is also important to clarify the relationship between gait asymmetry and velocity. A common view is that the topic of gait asymmetry poststroke has been investigated extensively. In fact, relatively few investigations (⬍10) have focused specifically on the nature and implications of asymmetry, and most had relatively small sample sizes.8-10,12,13,20 One study by Lin et al21 with a larger sample size (N⫽68) showed the importance of ankle impairment on gait characteristics but did not associate velocity and symmetry. Overall, it is difficult to judge both the prevalence of gait asymmetry poststroke and its specific association with velocity. As a result, the objectives of this study were to determine the prevalence and severity of asymmetry among independently ambulating stroke survivors and to establish the association between asymmetry and velocity.
METHODS Participants Participants were included if they had sustained a unilateral stroke (hemorrhagic or ischemic) 4 months or more previously and were capable of independent walking. Independent walking was defined as the ability to walk without supervision but could involve the use of a gait aid such as a cane or walker. Participants were excluded if they were unable to follow verbal requests. A convenience sample of healthy participants was also recruited. This study was approved by the Research Ethics Board at Sunnybrook Health Sciences Centre, and all participants provided written informed consent. Measurements Clinical assessment. The Chedoke-McMaster Stroke Assessment (CMSA) is a 2-part measure consisting of an impairment inventory and a disability inventory. The purpose of the impairment inventory is to determine the severity of physical impairments to classify stroke patients. It is divided into 6 dimensions, each measured with a 7-point scale.22,23 Smaller scores indicate greater motor impairment. The CMSA has good intrarater and interrater reliability and good concurrent validity with the Fugl-Meyer Assessment.22,23 The foot and leg dimensions of the CMSA, used as a measure of impairment in the current study, were administered to a subset of the larger group by either a physiotherapist with 13 years of experience or a trained research assistant. The average time between impairment testing and overground gait assessment was approximately 14 days. Spatiotemporal gait measures. Spatiotemporal parameters of gait were measured using a pressure-sensitive mat. The GAITRite mata is 366cm long by 81cm wide and contains a grid of 48⫻288 sensors (total of 13,824 sensors), arranged 1.27cm on center. The system records footfalls by the location of activated sensors and the time of activation and/or deactivation. Data were sampled at 30Hz and stored in a personal computer that calculated spatial and temporal parameters using application software. Task Protocol Participants walked across a level walkway over the pressure-sensitive mat (GAITRite) under 2 conditions: (1) at their preferred, comfortable speed and (2) at the fastest possible speed at which they felt safe. The healthy participants also completed these 2 walking tasks. Three trials were recorded for each condition and stored for offline analysis. Statistical Analysis The GAITRite system automatically calculates a variety of spatiotemporal measures including gait velocity step length, step time, swing time, and stance time. Output from the application software was opened in a spreadsheet using Excelb for further calculations. All values were averaged over the 3 trials for both preferred and fast-pace walking. In the case where participants were unable or unwilling to walk at a faster speed, the preferred velocity was also considered to be the fastest velocity. Temporal and spatial gait symmetry ratios were then calculated for each participant for both the preferred and fast walking using the appropriate mean swing and stance values in seconds and right and left step length values in centimeters. The following ratios for temporal symmetry were calculated: Temporal swing symmetry ⫽ paretic swing time/nonparetic swing time Arch Phys Med Rehabil Vol 89, February 2008
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Temporal stance symmetry ⫽ paretic stance time/nonparetic stance time Temporal swing-stance symmetry ⫽ swing time/stance time (for both paretic and nonparetic limbs) Overall temporal symmetry ⫽ paretic swing-stance symmetry/nonparetic swing-stance symmetry The spatial symmetry ratio was calculated as follows: Spatial step symmetry ⫽ nonparetic step length/paretic step length Statistical analysis was performed using SAS.c Descriptive statistics including mean and standard deviation (SD) were calculated for the entire group of participants and for symmetry subgroups (defined below) for the following: demographic data, gait velocity, all symmetry ratios (swing, stance, overall, spatial) percentage changes, and absolute percentage changes (from preferred to fast walking speed) for gait velocity and symmetry ratios. Prevalence of Gait Asymmetry The prevalence of asymmetry among the study participants was determined by classifying participants as either asymmetric or symmetric (both temporally and spatially) with respect to a 95% confidence interval (CI) created around the mean symmetry value for the overground walking of 24 healthy adults (young controls: age range, 24 –50y; mean, 32.87⫾6.36y; older group: age range, 52– 66y; mean, 59.22⫾3.99y). There were no age-related differences with respect to symmetry, so the data for the healthy participants were pooled. For the purposes of this study, a normative range for temporal symmetry was assumed to be 0.9 to 1.1.24,25 An overall temporal symmetry value greater than 1 indicates a preference to rely on the nonparetic limb during walking. The method of measuring symmetry may have an impact on the prevalence. Therefore, a measure of spatial symmetry, which we termed spatial step symmetry, was also examined. The relationships of spatial step symmetry to the various tem-
poral symmetry ratios were determined using the Pearson correlation (r). Correlations were also calculated between overall temporal symmetry and both swing and stance symmetry. Relationship Between Asymmetry, Walking Velocity, and Motor Impairment Correlations were calculated between preferred walking velocity and the overall temporal symmetry ratio and the spatial step symmetry ratio. A nonparametric correlation () was calculated between the CMSA leg and foot scores and the overall temporal symmetry ratio. Comparison of Temporal Symmetry Subgroups One-way analysis of variance (ANOVA) (3 levels) was performed to test for the effect of symmetry subgroup on preferred velocity and CMSA foot and leg scores. To address the concern that the CMSA scores are not interval data they were converted to ranked data before analysis. In all cases a level of P less than .05 was considered statistically significant. RESULTS A total of 54 participants were recruited as they presented to the Sunnybrook site of the Heart and Stroke Foundation Centre for Stroke Recovery. All participants performed the walking tasks without a gait aid to eliminate the potential influence of the aid on gait symmetry. Four participants wore an ankle-foot orthosis (AFO) during testing. A total of 24 healthy participants with no history of neurologic disorder or gait dysfunction were also recruited to serve as controls. Table 1 presents a summary of demographic data for the stroke survivors. The fast walking trials for 1 participant were discarded from analyses because there were not enough footfalls on the pressure-sensitive mat to reliably calculate spatiotemporal variables.
Table 1: Demographic Data and Spatiotemporal Gait Parameters for the Whole Group of Participants, the 3 Temporal Asymmetry Groups, and the Spatial Symmetric and Spatial Asymmetric Groups Whole Group
Parameters
(N⫽54)
Overall Temporal Symmetry Groups Normative (n⫽24) (0.9–1.1)
Mild (n⫽12) (1.1–1.5)
Severe (⫽18) (⬎1.5)
Spatial Symmetry Groups Symmetric (n⫽36) (0.9–1.1)
Asymmetric (n⫽18) (⬎1.1)
Participant demographics Age (y) 59.8⫾13.6 63.0⫾13.0 57.000⫾17.1 57.8⫾11.7 61.3⫾11.2 57.0⫾17.5 Months poststroke 49.90⫾64.20 48.10⫾83.70 39.60⫾24.70 59.30⫾52.89 51.92⫾72.27 45.97⫾45.41 Right hemiplegia (%) 57.4 62.5 50.0 55.6 58.3 55.6 Left hemiplegia (%) 42.6 37.5 50.0 44.4 41.7 44.4 CMSA foot 4.4⫾1.8 (n⫽37) 5.7⫾1.5 (n⫽12) 5.0⫾1.2 (n⫽10) 2.9⫾1.1 (n⫽15) 4.7⫾1.8 (n⫽24) 3.3⫾1.2 (n⫽12) CMSA leg 5.2⫾1.2 (n⫽37) 6.1⫾0.9 (n⫽12) 5.5⫾0.7 (n⫽10) 4.3⫾1.2 (n⫽15) 5.3⫾1.3 (n⫽24) 4.5⫾1.0 (n⫽13) Male (%) 64.8 66.7 91.7 44.4 61.1 72.2 Female (%) 35.2 33.3 8.3 55.6 38.9 27.8 Spatiotemporal gait parameters Preferred velocity (cm/s) 75.41⫾34.77 92.54⫾30.85 91.59⫾25.68 41.79⫾16.07 85.00⫾33.79 56.19⫾28.83 Preferred swing symmetry 1.32⫾0.49 1.02⫾0.04 1.17⫾0.05 1.82⫾0.60 1.17⫾0.27 1.61⫾0.70 Preferred stance symmetry 0.91⫾0.11 1.00⫾0.02 0.91⫾0.02 0.80⫾0.10 0.94⫾0.11 0.86⫾0.09 Preferred overall symmetry 1.51⫾0.70 1.02⫾0.05 1.29⫾0.07 2.30⫾0.70 1.30⫾0.51 1.92⫾0.86 Preferred step symmetry 1.08⫾0.80 1.01⫾0.07 1.00⫾0.11 1.24⫾1.40 0.99⫾0.05 1.28⫾1.39 Fast velocity (cm/s) 100.62⫾46.92 124.75⫾41.49 121.00⫾30.42 52.62⫾23.09 118.07⫾42.26 60.28⫾29.35 Fast swing symmetry 1.25⫾0.31 1.00⫾0.04 1.16⫾0.06 1.65⫾0.21 1.14⫾0.25 1.51⫾0.28 Fast stance symmetry 0.91⫾0.10 0.99⫾0.02 0.91⫾0.04 0.80⫾0.08 0.95⫾0.07 0.81⫾0.09 Fast overall symmetry 1.43⫾0.54 1.01⫾0.05 1.27⫾0.12 2.10⫾0.44 1.22⫾0.39 1.91⫾0.55 Fast step symmetry 1.09⫾0.81 1.01⫾0.06 0.98⫾0.11 1.27⫾1.43 0.99⫾0.05 1.30⫾1.48 NOTE. Values are mean ⫾ SD or as indicated. Arch Phys Med Rehabil Vol 89, February 2008
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Fig 1. A between-subject comparison illustrating the positive correlation between overall temporal symmetry and temporal swing symmetry (solid diamonds) at the preferred velocity (rⴝ.94, dfⴝ52, P<.001) and temporal stance symmetry (open squares) at the preferred velocity (rⴝ ⴚ.77, dfⴝ52, P<.001).
5.00 4.50 4.00 Overall symmetry (ratio)
Prevalence of Gait Asymmetry Overall 30 (55.5%) of the 54 subjects with chronic stroke showed evidence of statistically significant temporal asymmetry. It is important to note that all subjects with temporal asymmetry that exceeded the normative band had a ratio greater than 1 (ie, increased stance time on the nonparetic limb). Please refer to table 1 for group swing, stance, and overall temporal symmetry mean values at the preferred and fast speeds. The association between overall temporal symmetry and temporal swing symmetry is represented by a positive correlation (r⫽.94, df⫽52, P⬍.001). The association between overall temporal symmetry and temporal stance symmetry is represented by a negative correlation (r⫽⫺.77, df⫽52, P⬍.001) (fig 1). Mean values for spatial step symmetry at the preferred and fast velocities are summarized in table 1. Only 18 (33.3%) of the 54 participants exhibited a spatial step symmetry ratio outside the normative range of 0.9 to 1.1 (fig 2). It should be noted that 11 (61.1%) of these 18 subjects were classified as severely asymmetric temporally (classification described later). Spatial step symmetry ratio was not associated with overall temporal asymmetry (r⫽.03, df⫽52, P⫽.80) or preferred walking velocity (r⫽⫺.146, df⫽52, P⫽.292). In light of these results, the current study restricts its focus to the overall ratio of temporal asymmetry, because more participants exhibited temporal rather than spatial asymmetry. On the basis of the distribution of the overall temporal symmetry ratio we divided the group into 3 subgroups for the purposes of additional analysis: (1) normative (0.9 –1.1), (2) mild (1.1–1.5), and (3) severe (⬎1.5). This subdivision was based on the overall temporal symmetry at the preferred walking velocity. Although somewhat arbitrary, the cutoff value of 1.5 has some justification. Preliminary observations from ongoing work in our clinics have shown that physiotherapists can consistently detect the presence of temporal asymmetry among people with a symmetry index of 1.5 or greater. Values between 1.1 and 1.5 were more difficult to detect through observational approaches. Table 1 summarizes these 3 temporal symmetry categories (including demographics, mean velocity, symmetry ratios) that will be used to describe the data from this point forward.
3.50 Normative 3.00
Mild
2.50
Severe
2.00 1.50 1.00 0.50 0.00 0.00
20.00
40.00
60.00
80.00
100.00
120.00
140.00
160.00
Walking velocity (cm/s)
Fig 2. A between-subject comparison illustrating the negative correlation between preferred walking velocity and the overall temporal symmetry ratio at this speed (rⴝⴚ.583, dfⴝ52, P<.001). Each object represents 1 of the 54 participants and each shape represents a temporal symmetry category: severe asymmetry (triangles), mild asymmetry (squares) and normative symmetry (diamonds). Horizontal dashed lines represent the normative range for temporal symmetry (0.9 –1.1) based on a 95% CI around the mean temporal symmetry for 24 healthy control participants walking overground. Objects highlighted by a circle represent those subjects who also displayed spatial step asymmetry.
Relationship Between Asymmetry and Walking Velocity For between-subject comparisons, the mean preferred velocity for the entire group was 75.41⫾34.77cm/s. Mean fast velocity was 100.62⫾46.93cm/s (see table 1). There were 8 participants who could not increase their gait velocities on request. Three of these subjects had normative temporal symmetry and 5 exhibited severe temporal asymmetry at the preferred velocity. As mentioned above, in these cases the value of the preferred velocity was taken as the fastest gait velocity as well. The overall association between preferred walking velocity and overall temporal symmetry is represented by a statistically significant negative correlation (r⫽⫺.583, df⫽52, P⬍.001). Although there was a clear association between velocity and overall temporal symmetry, this was most strongly distinguished in those subjects with a much slower velocity. From visual inspection of the data it appears that those with a preferred velocity less than 60cm/s are more likely to exhibit severe overall temporal asymmetry (see fig 2). The mean overall symmetry of these slow walkers is 2.1⫾0.8 (range, 0.92– 4.52). All 4 subjects who wore an AFO during testing exhibited severe temporal asymmetry (range, 1.60 –2.57), and all but 1 of these subjects had a preferred gait velocity less than 60cm/s (range, 22.15– 86.53cm/s). Therefore, the 3 AFO users with gait speeds less than 60cm/s are nondescript within the severely asymmetric group in figure 2. The AFO user with a gait velocity of 86.53cm/s is distinct from the other participants with similar walking speeds (ie, 80 –95cm/s) in that that participant exhibited the largest overall temporal symmetry ratio (1.60), albeit not by a great amount. One-way ANOVA results showed a main effect of temporal symmetry group (normative, mild, severe) for preferred velocity (F⫽23.21, P⬍.001). Tukey analysis showed that the significant differences in mean preferred velocity were between the severe asymmetry group and both the normative symmetry and mild asymmetry groups. The mean preferred velocity was not significantly different between the mild asymmetry and normative symmetry groups. Arch Phys Med Rehabil Vol 89, February 2008
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GAIT ASYMMETRY AFTER STROKE, Patterson Table 2: The Effects of Increased Gait Velocity on Temporal Symmetry No Change
No Increase
Group
% of Group
Improved Symmetry Ratio Mean Change in Symmetry
% of Group
Worse Symmetry Ratio Mean Change in Symmetry
% of Group
% of Group
Whole (N⫽53) Normative symmetry (n⫽23) Mild asymmetry (n⫽12) Severe asymmetry (n⫽18)
50.9 34.8 66.7 61.1
10.05⫾13.39 4.40⫾2.57 7.78⫾6.38 15.82⫾19.15
32.1 47.8 33.3 11.1
8.24⫾10.51 5.57⫾5.00 3.73⫾3.43 31.99⫾13.96
1.9 4.3 0.0 0.0
15.1 13.0 0.0 27.8
NOTE. Values are mean ⫾ SD for the percentage change in symmetry (improved or worse) with increased velocity and the percentage of subjects within each group who exhibited the specified effect of increased gait velocity on temporal asymmetry as follows: improved, worsened, no change (indicates no change in symmetry with increased speed), and no increase (indicates those participants who were unable to increase the gait velocity above the preferred speed).
DISCUSSION The results illustrate that profound overall temporal asymmetry can be found in many stroke patients classified as independent ambulators. In this study, more than half (55.5%) of the participants exhibited temporal asymmetry. By comparison, fewer poststroke patients (33.3%) exhibited spatial step asymmetry. There is significant variation in temporal symmetry values within this functionally homogeneous group. Symmetry ratios ranged from within the normative range (0.9 –1.1) to Arch Phys Med Rehabil Vol 89, February 2008
A 5.00 4.50 4.00
Normative 3.50
Overall symmetry (ratio)
Relationship Between Asymmetry and Motor Impairment It is possible that the slow velocity and degree of asymmetry can be simply linked to the degree of limb impairment. If this were true then the index of limb impairment (CMSA) would be sufficient to express the expected variation in asymmetry and its relationship to velocity. Temporal symmetry appears partially related to motor impairment as measured by the CMSA. These significant negative correlations between the overall temporal symmetry ratio and CMSA scores for the foot (r⫽⫺.628, df⫽35, P⬍.001) and leg (r⫽⫺.644, df⫽35, P⬍.001) are depicted in figure 3. These relationships were particularly evident for subjects with preferred overall temporal symmetry values of 1.5 or higher (severe temporal asymmetry). One-way ANOVA results showed a main effect of temporal symmetry group (normative, mild, severe) for CMSA leg (F⫽12.42, P⬍.001) and foot scores (F⫽18.13, P⬍.001). Tukey analysis showed that the CMSA leg and foot scores were significantly different between the severe asymmetry group and both the normative symmetry and mild asymmetry groups. The CMSA leg and foot scores were not significantly different between the mild asymmetry and normative symmetry groups. Mean CMSA leg and foot scores are summarized in table 1.
severely asymmetric (4.52). This finding is consistent with that of Wall and Turnbull,10 who noted variation in asymmetry within a group of 25 “functionally ambulant” chronic stroke patients. Grouping persons with chronic stroke according to
Mild Severe
3.00 2.50 2.00 1.50 1.00 0.50 0.00 0
1
2
3
4
5
6
7
Foot impairment (CMSA foot score 0-7)
B 5.00 4.50 4.00 Overall symmetry (ratio)
Within-subject comparisons. In addition to the clear between-subject differences in walking velocity (associated with symmetry), there were also within-subject differences when comparing preferred and fast walking speeds. Twenty-seven (50.9%) of the 53 participants exhibited an improved temporal symmetry ratio (ie, moved closer to 1) at the fast velocity compared with the temporal symmetry ratio at the preferred velocity. Seventeen (32.1%) participants exhibited a worse temporal symmetry ratio or increased asymmetry (ie, moved further from 1) with increased walking velocity. The mean absolute percentage change in the overall temporal symmetry ratio for the entire group was 7.78%⫾11.69% when subjects walked faster. There appears to be between-subject and between-group differences in terms of the effect of increased walking velocity on overall temporal symmetry. These changes in symmetry are summarized in table 2.
3.50
Normative Mild Severe
3.00 2.50 2.00 1.50 1.00 0.50 0.00 0
1
2
3
4
5
6
7
Leg impairment (CMSA leg score 0-7)
Fig 3. Between-subject comparisons illustrating the negative correlation between the overall temporal symmetry ratio at the preferred gait speed and (A) CMSA foot score (rⴝ ⴚ.628, dfⴝ35, P<.001) and (B) CMSA leg score (rⴝ ⴚ.644, dfⴝ35, P<.001). Each shape represents a temporal symmetry category, severe asymmetry (triangles), mild asymmetry (squares), and normative symmetry (diamonds).
GAIT ASYMMETRY AFTER STROKE, Patterson
overall temporal symmetry at the preferred speed appears to have some merit in light of the complex relationship of temporal symmetry to motor impairment and gait velocity. Although use of CMSA scores and velocity alone can distinguish between people at the extremes of the spectrum (ie, fast and slow walkers, good and poor motor recovery), this approach does not distinguish among all poststroke ambulators, particularly those in the midrange (ie, velocity between 60 –100cm/s and CMSA scores between 4 – 6). With respect to the association between measures, spatial step asymmetry does not appear to correlate with temporal asymmetry or gait velocity. Although less prevalent, spatial step asymmetry appears more likely to occur in stroke survivors who exhibit severe temporal asymmetry compared with survivors who fall in the mild asymmetry or normative symmetry groups. Previous work has presented conflicting information regarding the relationship of gait speed and various measures of temporal symmetry.9,12 The current study clearly shows a relationship. However, it appears to be a nonlinear association in which greater degrees of asymmetry are associated with very slow walking speeds (⬍60cm/s). Such complexity of association may have influenced the ability to show such an association with smaller sample sizes or narrower ranges of patient abilities. There was a different association between temporal symmetry and walking velocity when comparing within individual participants. Those who are severely asymmetric appear more likely to exhibit improved temporal symmetry at their fast walking speeds. In contrast, those participants within the normative and mild asymmetry groups were equally likely to exhibit increased or decreased temporal asymmetry at a faster gait speed. It is not yet known whether these observed changes in temporal symmetry associated with increased gait speed are clinically significant. It is possible that the effect of increased velocity on temporal symmetry may depend on the specific underlying impairment causing the temporal asymmetry. The overall gait symmetry ratio in hemiplegic persons represents an increase in paretic swing duration and a decrease in paretic stance duration. Two possible impairments might lead to this pattern of asymmetry. First, an inability to generate sufficient muscle power to swing the paretic limb through quickly enough would result in prolonged swing duration for that limb.10 In this case, an increase in velocity would lead to a decrease in the amount of time available to swing the paretic limb through, thereby exacerbating the situation and resulting in a worsening of the temporal asymmetry. Alternatively, impaired balance that results in an inability to control the center of mass over the paretic limb could lead a person to shorten stance duration on this limb.10 In this situation, an increase in velocity would naturally lead to decreased time spent in the paretic stance, which may not affect the temporal symmetry ratio or could lead to an improvement in the symmetry ratio. Overall temporal symmetry also appears to be related to motor impairment of the leg and foot as measured by the CMSA. These findings correspond with previous studies using different measures of motor impairment (specifically, Brunnstrom stages and Fugl-Meyer Assessment).9,13 Similar to its relationship with velocity, the current study shows that the relationship of temporal symmetry and motor impairment is particularly evident for subjects who were severely asymmetric (ratios ⱖ1.5). Subjects with less motor impairment (CMSA leg scores of 6 and 7) may or may not exhibit temporally asymmetric gait. As mentioned above, although CMSA scores can distinguish among some stroke survivors, there are potentially important differences in poststroke gait not easily determined from
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CMSA scores alone. This is particularly true for those people in the middle range of motor function. It is possible that in the case of severe temporal asymmetry, gait function is heavily influenced by the degree of motor impairment, particularly in the leg. This may serve to limit a person’s capacity for forward progression during gait such that slow gait speed is an unavoidable consequence of severe temporal asymmetry. Those people exhibiting mild or moderate temporal asymmetries may have sufficient motor recovery in the lower limb to enable compensatory strategies to increase gait speed with varying degrees of success. In these cases, other factors beyond motor impairment—for example, dynamic balance control—may be more important determinants of walking competency. Clinical Relevance of Gait Asymmetry Although gait velocity is reflective of gait performance it does not, as identified by Olney et al,6 have “explicative capacity.” Used in isolation, gait speed neither assists in understanding the nature of poststroke gait deficits nor does it direct treatment.6 In addition, gait speed as a clinical outcome measure does not reflect components of a gait rehabilitation program related to training equal weight bearing and weight shifting. A measure of temporal gait symmetry included in quantitative gait analysis might better reflect this aspect of rehabilitation. It appears that the overall temporal symmetry ratio is superior to both swing and stance ratios as well as spatial symmetry ratios in discriminating among poststroke ambulators. Several studies have cited thresholds for gait velocity as a means of predicting ambulatory function. Holden et al26 identified 60cm/s, based on their review of the literature, as the minimum velocity needed for “a reasonable degree of functional independence,” defined as the ability to ambulate over all surfaces and all stairs. Perry et al27 cited 42cm/s as the cutoff for community ambulation. However, gait velocity when used alone is often insufficient in discriminating among poststroke ambulators. Perry27 noted that velocity alone failed to distinguish between the various levels of household ambulators. Taylor et al28 noted that gait velocity measured in the clinic was predictive of gait velocity in the community only for those with gait speeds greater than 80cm/s. The current results suggest that a measure of temporal symmetry may assist in further discrimination of poststroke ambulators, particularly those with gait speeds less than 60cm/s. Within this group, the overall temporal symmetry values cover a range of 3.6 (0.92– 4.52). In contrast, the range of overall temporal symmetry ratios for people with a preferred velocity greater than 60cm/s was only 0.65 (0.95–1.60). Specifically, classification of poststroke ambulators (particularly those who walk slower than 60cm/s) as exhibiting normative symmetry, mild asymmetry, or severe asymmetry may provide additional information regarding their gait performances. However, what needs to be determined now is the clinical relevance of these classifications. The functional implications of either immediate changes in temporal asymmetry with increased gait speed or long-term changes in temporal asymmetry with rehabilitation interventions are not yet known. Study Limitations This study focused on community-dwellers with chronic stroke, and therefore the results may not be generalizable to stroke patients in the acute stage or to people who need assistance for ambulation. In addition, the cross-sectional design of this study would not show changes in gait symmetry (and its relationship to velocity) that may occur within a person over Arch Phys Med Rehabil Vol 89, February 2008
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time. Finally, as noted previously, future work will need to link the degree of gait asymmetry to clinically relevant outcomes to better establish the clinical significance of such observations. CONCLUSIONS Roth et al12 suggested that a measure of temporal symmetry should be included in a comprehensive gait evaluation because they found that velocity did not correlate significantly with symmetry. We certainly agree with the view that gait symmetry ratio should be included as a measure of gait after stroke, even though the present study did show an association between symmetry and velocity. Although the specific nature of the association between symmetry and walking velocity is more complex than the linear model presently used, the current work emphasizes a potential link between disorders of control showed by asymmetry and the capacity to walk more quickly. Although velocity of walking certainly has implications for functional activities, there are many more potential consequences associated with gait asymmetry (challenges to dynamic balance control, increased risk of cumulative musculoskeletal injury, gait inefficiencies, limitations on walking speed). The findings of the present study and the importance of gait symmetry leads us to the view that gait symmetry should be the primary focus of poststroke assessment and that walking speed should serve as a complementary measure. It is our view that the ease of measurement, rather than clinical value, has led to the emphasis on measures such as gait velocity. New, clinically viable measurement approaches are emerging that can make the assessment of gait in rehabilitation settings more valuable to the clinician and patient. A clinical community more focused on important outcomes such as gait symmetry would further stimulate the development of simple cost-effective measurement solutions. References 1. Bohannon RW, Andrews AW, Smith MB. Rehabilitation goals of patients with hemiplegia. Int J Rehabil Res 1988;11:181-3. 2. Flansbjer U-B, Holmback AM, Downham D, Patten C, Lexell J. Reliability of gait performance tests in men and women with hemiparesis after stroke. J Rehabil Med 2005;37:75-82. 3. Macko RF, Ivey FM, Forrester LW, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke. A randomized, controlled trial. Stroke 2005;36:2206-11. 4. Mizrahi J, Susak Z, Heller I, Najenson T. Variation of timedistance parameters of the stride as related to clinical gait improvement in hemiplegics. Scand J Rehabil Med 1982;14:133-40. 5. Lord SE, Halligan PW, Wade DT. Visual gait analysis: the development of a clinical assessment and scale. Clin Rehabil 1998; 12:107-19. 6. Olney SJ, Griffin MP, McBride ID. Temporal, kinematic and kinetic variables related to gait speed in subjects with hemiplegia: a regression approach. Phys Ther 1994;74:872-85. 7. Kim CM, Eng JJ. Symmetry in vertical ground reaction force is accompanied by symmetry in temporal but not distance variables of gait in persons with stroke. Gait Posture 2003;18:23-8. 8. Bohannon RW. Gait performance of hemiparetic stroke patients: selected variables. Arch Phys Med Rehabil 1987;68:777-81. 9. Brandstater ME, deBruin H, Gowland C, Clarke BM. Hemiplegic gait: analysis of temporal variables. Arch Phys Med Rehabil 1983;64:583-7.
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10. Wall JC, Turnbull GI. Gait asymmetries in residual hemiplegia. Arch Phys Med Rehabil 1986;67:550-3. 11. Griffin MP, Olney SJ, McBride ID. Role of symmetry in gait performance of stroke subjects with hemiplegia. Gait Posture 1995;3:132-42. 12. Roth EJ, Merbitz C, Mroczek K, Dugan SA, Suh WW. Hemiplegic gait: relationships between walking speed and other temporal parameters. Am J Phys Med Rehabil 1997;76:128-33. 13. Hsu AL, Tang PF, Jan MH. Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild to moderate stroke. Arch Phys Med Rehabil 2003;84:1185-93. 14. Davis BL, Ortolano M, Richards K, Redhed J, Kuznicki J, Sahgal V. Realtime visual feedback diminishes energy consumption of amputee subjects during treadmill locomotion. J Prosthet Orthot 2004;16:49-54. 15. Draper ER. A treadmill-based system for measuring symmetry of gait. Med Eng Phys 2000;22:215-22. 16. Platts MM, Rafferty D, Paul L. Metabolic cost of overground gait in younger stroke patients and healthy controls. Med Sci Sports Exerc 2006;38:1041-6. 17. Michael KM, Allen JK, Macko RF. Reduced ambulatory activity after stroke: the role of balance, gait and cardiovascular fitness. Arch Phys Med Rehabil 2005;86:1552-6. 18. Nolan L, Wit A, Dudzinski K, Lees A, Lake M, Wychowanski M. Adjustments in gait symmetry with walking speed in transfemoral and trans-tibial amputees. Gait Posture 2003;17:142-51. 19. Norvell DC, Czerniecki JM, Reiber GE, Maynard C, Pecoraro JA, Weiss NS. The prevalence of knee pain and symptomatic knee osteoarthritis among veteran traumatic amputees and nonamputees. Arch Phys Med Rehabil 2005;86:487-93. 20. Chen G, Patten C, Kothari DH, Zajac FE. Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds. Gait Posture 2005;22:51-6. 21. Lin P, Yang Y, Cheng S, Wang R. The relation between ankle impairments and gait velocity and symmetry in people with stroke. Arch Phys Med Rehabil 2006;87:562-8. 22. Gowland C, VanHullenaar S, Torresin W. Chedoke-McMaster Stroke Assessment: development, validation and administration manual. Hamilton: McMaster Univ; 1995. 23. Gowland C, Stratford P, Ward M, et al. Measuring physical impairment and disability with the Chedoke-McMaster stroke assessment. Stroke 1993;24:58-63. 24. Cohen E. Gait asymmetry and step to step variability post stroke [dissertation]. Toronto: Univ Toronto; 2004. 25. Patterson KK. Characteristics of independent ambulation in chronic stroke survivors. [dissertation]. Toronto: Univ Toronto; 2006. 26. Holden MK, Gill KM, Magliozzi MR. Gait assessment for neurologically impaired patients. Standards for outcome assessment. Phys Ther 1986;66:1530-9. 27. Perry J, Garrett M, Gronley JK, Mulroy SJ. Classification of walking handicap in the stroke population. Stroke 1995;26:982-9. 28. Taylor D, Stretton CM, Mudge S, Garrett N. Does clinic-measured gait speed differ from gait speed measured in the community in people with stroke? Clin Rehabil 2006;20:438-44. Suppliers a. CIR Systems, 1180 US Hwy 46, Parsippany, NJ 07054. b. Version 2003; Microsoft Corp, One Microsoft Way, Redmond, WA 98052. c. Version 9.1; SAS Institute Inc, 100 SAS Campus Dr, Cary, NC 27513.
ORIGINAL ARTICLE
Gait Asymmetry in Community-Ambulating Stroke Survivors Kara K. Patterson, MSc, Iwona Parafianowicz, Cynthia J. Danells, MSc, Valerie Closson, MSc, Mary C. Verrier, MHSc, W. Richard Staines, PhD, Sandra E. Black, MD, PhD, William E. McIlroy, PhD ABSTRACT. Patterson KK, Parafianowicz I, Danells CJ, Closson V, Verrier MC, Staines WR, Black SE, McIlroy WE. Gait asymmetry in community-ambulating stroke survivors. Arch Phys Med Rehabil 2008;89:304-10. Objectives: To determine the prevalence and severity of asymmetry among independently ambulating stroke survivors and to establish the association between velocity and asymmetry. Design: Descriptive analysis. Setting: Research gait laboratory in a Canadian hospital. Participants: Community-dwelling, independently ambulating participants (N⫽54) with chronic stroke. Interventions: Not applicable. Main Outcome Measures: Overground gait velocity, symmetry ratios for temporal and spatial step parameters, and motor impairment of the foot and leg. Spatiotemporal parameters were collected with a pressure-sensitive mat. Motor impairment was measured clinically with the Chedoke-McMaster Stroke Assessment. Results: Thirty (55.5%) participants showed statistically significant temporal asymmetry and 18 (33.3%) exhibited statistically significant spatial asymmetry. Preferred velocity was negatively associated with temporal asymmetry (r⫽ ⫺.583, df⫽52, P⬍.001) but not spatial asymmetry (r⫽⫺.146, df⫽52, P⫽.29). Temporal asymmetry was also associated with motor recovery of the leg (r⫽ ⫺.644, df⫽35, P⬍.001) and foot (r⫽ ⫺.628, df⫽35, P⬍.001). Conclusions: The results of the current study illustrate that temporal asymmetry can be found in many independently ambulating stroke patients. The work highlights the need for a standard assessment of poststroke gait symmetry in light of the complex relationship with motor impairment and velocity. Key Words: Cerebrovascular accident; Gait disorders, neurologic; Rehabilitation. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
From the Heart and Stroke Foundation Centre for Stroke Recovery, Sunnybrook Health Sciences Centre, Toronto, ON, Canada (Patterson, Parafianowicz, Danells, Closson, Staines, Black, McIlroy); Toronto Rehabilitation Institute, Toronto, ON, Canada (Patterson, Verrier, Staines, McIlroy); Graduate Department of Rehabilitation Science, University of Toronto, Toronto, ON, Canada (Patterson, Verrier, Black, McIlroy); Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada (Staines, McIlroy); and Department of Physical Therapy, University of Toronto, Toronto, ON, Canada (Verrier). Supported by the Toronto Rehabilitation Institute, Marguerite Harland Smith Bursary, Lois Snelling Bursary, and the Canadian Institutes of Health Research (grant no. MOP62957). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to William E. McIlroy, PhD, Faculty of Applied Health Sciences, University of Waterloo, 200 University Ave W, Waterloo, ON N2L 3G1, Canada, e-mail: [email protected]. 0003-9993/08/8902-00318$34.00/0 doi:10.1016/j.apmr.2007.08.142
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TROKE IS THE LEADING CAUSE of adult neurologic S disability affecting all aspects of life including mobility, activities of daily living, communication, and cognition. Gait deficits greatly contribute to functional disability after stroke, and of all stroke-related impairments, improvement of walking function is the goal most often stated by stroke patients.1 In light of the importance of gait, considerable attention has been focused on the measurement and improvement of gait velocity in persons with stroke.2-4 As a clinical measure, velocity reflects overall gait performance; however, it is limited in both its value to document poststroke recovery and the information it provides regarding the underlying impairments.5,6 In addition, gait velocity does not fully reflect all aspects of a typical stroke rehabilitation program and thus is limited as a solitary clinical measure to direct treatment and to reflect its outcomes. For example, in addition to increasing gait speed, considerable focus is placed on the equalization of weight bearing through the lower extremities and the capacity to shift weight between the lower extremities during gait.7,8 A complementary measure that may better reflect this particular aspect of rehabilitation is gait symmetry. Brandstater et al9 suggested that symmetry may characterize poststroke gait better than unilateral values. Normative gait tends to be symmetric both spatially (between left and right joint angles, step and stride lengths) and temporally (between right and left swing, stance, step and stride times), with interlimb differences in vertical force and temporal parameters less than 6%.7 In contrast, the unilateral deficits that occur after stroke are likely to result in gait asymmetry. Such asymmetry has been shown by measurement of limb-specific differences in kinematic and kinetic measures of gait as well as differences in overall spatiotemporal characteristics such as swing and stance times.10,11 Studies examining the symmetry of spatiotemporal parameters have described a gait pattern associated with a favoring of the paretic limb.10 That is, compared with the nonparetic lower extremity, swing phase duration is prolonged and single-limb support time is shortened on the paretic limb.9,10 A specific interest in the present study was the relationship between these 2 important aspects of gait recovery: symmetry and velocity. There have only been 2 studies that have specifically explored this relationship, and in both cases the studies primarily focused on temporal measures of gait for the index of symmetry.9,12 Unfortunately, the results from these studies are conflicting about the relationship between specific measures of gait symmetry and walking velocity. Roth et al12 found that while temporal gait components (swing symmetry and swing/ stance ratio in the paretic limb) were linearly correlated with walking velocity, overall temporal symmetry (paretic swing and/or paretic stance:nonparetic swing and/or nonparetic stance) was not related to velocity. On the other hand, Brandstater9 found that overall temporal symmetry was related to velocity. There is concern that the conflicting results of these studies may be attributed to relatively small sample sizes (⬍25 subjects). These studies may also be limited by the possibility that some subjects were permitted the use of canes, which may have had a profound impact on the symmetry-velocity relationship in some people.
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It is our view that gait velocity and temporal asymmetry are related, given that both features of poststroke gait correlate with the same impairment measures. Both gait velocity and temporal asymmetry have been shown to correlate with motor recovery, lower-extremity muscle strength, peak torque, total work, and spasticity, albeit to varying degrees.8,9,13 It may be that poor temporal symmetry may be a primary determinant of a slow gait velocity because of the associated challenges linked to asymmetry (eg, asymmetric limb loading, inefficiency, challenged balance control). Regardless of the nature of its relationship to velocity, asymmetry is an important issue to address in the rehabilitation of poststroke gait for several possible reasons including efficiency, overall activity level, and musculoskeletal health. It is believed that gait symmetry and energy expenditure are related and that symmetric gait is the most efficient pattern.14,15 People poststroke have higher energy expenditure during gait and extremely low ambulatory activity levels compared with healthy controls.16,17 It is possible that the asymmetric pattern of poststroke gait contributes to the observed increased energy expenditure. It is also possible that asymmetric chronic stroke patients reduce their overall activity levels over time in response to the increased cost of this gait pattern. Asymmetric poststroke gait may also negatively affect the musculoskeletal health of the nonparetic limb. High forces repetitively applied to a limb can lead to pain and joint degeneration.18,19 In stroke survivors, temporal asymmetry positively correlates with increased vertical ground reaction forces through the nonparetic lower limb.7 Therefore, over time, the asymmetric gait of a stroke patient exposes the nonparetic limb to increased repetitive loading. To our knowledge, there are no studies that have examined the incidence of joint pain and degeneration in the stroke population. However, a few studies of the amputee population have reported an increased incidence of joint pain and degeneration and an increased risk for osteoarthritis in the intact limb of amputees.18,19 These musculoskeletal issues identified in the amputee population have been attributed to greater ground reaction forces through the intact limb compared with the amputated limb, associated with gait asymmetry.18,19 It seems reasonable to assume that the same asymmetric pattern seen in the stroke population could lead to the same musculoskeletal consequences in the nonparetic limb. In light of the potential long-term implications of persisting gait asymmetry (decreased efficiency, decreased activity level, musculoskeletal injury) and its possible use as an objective clinical gait measure, there is a need to better understand the occurrence and severity of asymmetry among ambulating stroke survivors. It is also important to clarify the relationship between gait asymmetry and velocity. A common view is that the topic of gait asymmetry poststroke has been investigated extensively. In fact, relatively few investigations (⬍10) have focused specifically on the nature and implications of asymmetry, and most had relatively small sample sizes.8-10,12,13,20 One study by Lin et al21 with a larger sample size (N⫽68) showed the importance of ankle impairment on gait characteristics but did not associate velocity and symmetry. Overall, it is difficult to judge both the prevalence of gait asymmetry poststroke and its specific association with velocity. As a result, the objectives of this study were to determine the prevalence and severity of asymmetry among independently ambulating stroke survivors and to establish the association between asymmetry and velocity.
METHODS Participants Participants were included if they had sustained a unilateral stroke (hemorrhagic or ischemic) 4 months or more previously and were capable of independent walking. Independent walking was defined as the ability to walk without supervision but could involve the use of a gait aid such as a cane or walker. Participants were excluded if they were unable to follow verbal requests. A convenience sample of healthy participants was also recruited. This study was approved by the Research Ethics Board at Sunnybrook Health Sciences Centre, and all participants provided written informed consent. Measurements Clinical assessment. The Chedoke-McMaster Stroke Assessment (CMSA) is a 2-part measure consisting of an impairment inventory and a disability inventory. The purpose of the impairment inventory is to determine the severity of physical impairments to classify stroke patients. It is divided into 6 dimensions, each measured with a 7-point scale.22,23 Smaller scores indicate greater motor impairment. The CMSA has good intrarater and interrater reliability and good concurrent validity with the Fugl-Meyer Assessment.22,23 The foot and leg dimensions of the CMSA, used as a measure of impairment in the current study, were administered to a subset of the larger group by either a physiotherapist with 13 years of experience or a trained research assistant. The average time between impairment testing and overground gait assessment was approximately 14 days. Spatiotemporal gait measures. Spatiotemporal parameters of gait were measured using a pressure-sensitive mat. The GAITRite mata is 366cm long by 81cm wide and contains a grid of 48⫻288 sensors (total of 13,824 sensors), arranged 1.27cm on center. The system records footfalls by the location of activated sensors and the time of activation and/or deactivation. Data were sampled at 30Hz and stored in a personal computer that calculated spatial and temporal parameters using application software. Task Protocol Participants walked across a level walkway over the pressure-sensitive mat (GAITRite) under 2 conditions: (1) at their preferred, comfortable speed and (2) at the fastest possible speed at which they felt safe. The healthy participants also completed these 2 walking tasks. Three trials were recorded for each condition and stored for offline analysis. Statistical Analysis The GAITRite system automatically calculates a variety of spatiotemporal measures including gait velocity step length, step time, swing time, and stance time. Output from the application software was opened in a spreadsheet using Excelb for further calculations. All values were averaged over the 3 trials for both preferred and fast-pace walking. In the case where participants were unable or unwilling to walk at a faster speed, the preferred velocity was also considered to be the fastest velocity. Temporal and spatial gait symmetry ratios were then calculated for each participant for both the preferred and fast walking using the appropriate mean swing and stance values in seconds and right and left step length values in centimeters. The following ratios for temporal symmetry were calculated: Temporal swing symmetry ⫽ paretic swing time/nonparetic swing time Arch Phys Med Rehabil Vol 89, February 2008
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Temporal stance symmetry ⫽ paretic stance time/nonparetic stance time Temporal swing-stance symmetry ⫽ swing time/stance time (for both paretic and nonparetic limbs) Overall temporal symmetry ⫽ paretic swing-stance symmetry/nonparetic swing-stance symmetry The spatial symmetry ratio was calculated as follows: Spatial step symmetry ⫽ nonparetic step length/paretic step length Statistical analysis was performed using SAS.c Descriptive statistics including mean and standard deviation (SD) were calculated for the entire group of participants and for symmetry subgroups (defined below) for the following: demographic data, gait velocity, all symmetry ratios (swing, stance, overall, spatial) percentage changes, and absolute percentage changes (from preferred to fast walking speed) for gait velocity and symmetry ratios. Prevalence of Gait Asymmetry The prevalence of asymmetry among the study participants was determined by classifying participants as either asymmetric or symmetric (both temporally and spatially) with respect to a 95% confidence interval (CI) created around the mean symmetry value for the overground walking of 24 healthy adults (young controls: age range, 24 –50y; mean, 32.87⫾6.36y; older group: age range, 52– 66y; mean, 59.22⫾3.99y). There were no age-related differences with respect to symmetry, so the data for the healthy participants were pooled. For the purposes of this study, a normative range for temporal symmetry was assumed to be 0.9 to 1.1.24,25 An overall temporal symmetry value greater than 1 indicates a preference to rely on the nonparetic limb during walking. The method of measuring symmetry may have an impact on the prevalence. Therefore, a measure of spatial symmetry, which we termed spatial step symmetry, was also examined. The relationships of spatial step symmetry to the various tem-
poral symmetry ratios were determined using the Pearson correlation (r). Correlations were also calculated between overall temporal symmetry and both swing and stance symmetry. Relationship Between Asymmetry, Walking Velocity, and Motor Impairment Correlations were calculated between preferred walking velocity and the overall temporal symmetry ratio and the spatial step symmetry ratio. A nonparametric correlation () was calculated between the CMSA leg and foot scores and the overall temporal symmetry ratio. Comparison of Temporal Symmetry Subgroups One-way analysis of variance (ANOVA) (3 levels) was performed to test for the effect of symmetry subgroup on preferred velocity and CMSA foot and leg scores. To address the concern that the CMSA scores are not interval data they were converted to ranked data before analysis. In all cases a level of P less than .05 was considered statistically significant. RESULTS A total of 54 participants were recruited as they presented to the Sunnybrook site of the Heart and Stroke Foundation Centre for Stroke Recovery. All participants performed the walking tasks without a gait aid to eliminate the potential influence of the aid on gait symmetry. Four participants wore an ankle-foot orthosis (AFO) during testing. A total of 24 healthy participants with no history of neurologic disorder or gait dysfunction were also recruited to serve as controls. Table 1 presents a summary of demographic data for the stroke survivors. The fast walking trials for 1 participant were discarded from analyses because there were not enough footfalls on the pressure-sensitive mat to reliably calculate spatiotemporal variables.
Table 1: Demographic Data and Spatiotemporal Gait Parameters for the Whole Group of Participants, the 3 Temporal Asymmetry Groups, and the Spatial Symmetric and Spatial Asymmetric Groups Whole Group
Parameters
(N⫽54)
Overall Temporal Symmetry Groups Normative (n⫽24) (0.9–1.1)
Mild (n⫽12) (1.1–1.5)
Severe (⫽18) (⬎1.5)
Spatial Symmetry Groups Symmetric (n⫽36) (0.9–1.1)
Asymmetric (n⫽18) (⬎1.1)
Participant demographics Age (y) 59.8⫾13.6 63.0⫾13.0 57.000⫾17.1 57.8⫾11.7 61.3⫾11.2 57.0⫾17.5 Months poststroke 49.90⫾64.20 48.10⫾83.70 39.60⫾24.70 59.30⫾52.89 51.92⫾72.27 45.97⫾45.41 Right hemiplegia (%) 57.4 62.5 50.0 55.6 58.3 55.6 Left hemiplegia (%) 42.6 37.5 50.0 44.4 41.7 44.4 CMSA foot 4.4⫾1.8 (n⫽37) 5.7⫾1.5 (n⫽12) 5.0⫾1.2 (n⫽10) 2.9⫾1.1 (n⫽15) 4.7⫾1.8 (n⫽24) 3.3⫾1.2 (n⫽12) CMSA leg 5.2⫾1.2 (n⫽37) 6.1⫾0.9 (n⫽12) 5.5⫾0.7 (n⫽10) 4.3⫾1.2 (n⫽15) 5.3⫾1.3 (n⫽24) 4.5⫾1.0 (n⫽13) Male (%) 64.8 66.7 91.7 44.4 61.1 72.2 Female (%) 35.2 33.3 8.3 55.6 38.9 27.8 Spatiotemporal gait parameters Preferred velocity (cm/s) 75.41⫾34.77 92.54⫾30.85 91.59⫾25.68 41.79⫾16.07 85.00⫾33.79 56.19⫾28.83 Preferred swing symmetry 1.32⫾0.49 1.02⫾0.04 1.17⫾0.05 1.82⫾0.60 1.17⫾0.27 1.61⫾0.70 Preferred stance symmetry 0.91⫾0.11 1.00⫾0.02 0.91⫾0.02 0.80⫾0.10 0.94⫾0.11 0.86⫾0.09 Preferred overall symmetry 1.51⫾0.70 1.02⫾0.05 1.29⫾0.07 2.30⫾0.70 1.30⫾0.51 1.92⫾0.86 Preferred step symmetry 1.08⫾0.80 1.01⫾0.07 1.00⫾0.11 1.24⫾1.40 0.99⫾0.05 1.28⫾1.39 Fast velocity (cm/s) 100.62⫾46.92 124.75⫾41.49 121.00⫾30.42 52.62⫾23.09 118.07⫾42.26 60.28⫾29.35 Fast swing symmetry 1.25⫾0.31 1.00⫾0.04 1.16⫾0.06 1.65⫾0.21 1.14⫾0.25 1.51⫾0.28 Fast stance symmetry 0.91⫾0.10 0.99⫾0.02 0.91⫾0.04 0.80⫾0.08 0.95⫾0.07 0.81⫾0.09 Fast overall symmetry 1.43⫾0.54 1.01⫾0.05 1.27⫾0.12 2.10⫾0.44 1.22⫾0.39 1.91⫾0.55 Fast step symmetry 1.09⫾0.81 1.01⫾0.06 0.98⫾0.11 1.27⫾1.43 0.99⫾0.05 1.30⫾1.48 NOTE. Values are mean ⫾ SD or as indicated. Arch Phys Med Rehabil Vol 89, February 2008
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Fig 1. A between-subject comparison illustrating the positive correlation between overall temporal symmetry and temporal swing symmetry (solid diamonds) at the preferred velocity (rⴝ.94, dfⴝ52, P<.001) and temporal stance symmetry (open squares) at the preferred velocity (rⴝ ⴚ.77, dfⴝ52, P<.001).
5.00 4.50 4.00 Overall symmetry (ratio)
Prevalence of Gait Asymmetry Overall 30 (55.5%) of the 54 subjects with chronic stroke showed evidence of statistically significant temporal asymmetry. It is important to note that all subjects with temporal asymmetry that exceeded the normative band had a ratio greater than 1 (ie, increased stance time on the nonparetic limb). Please refer to table 1 for group swing, stance, and overall temporal symmetry mean values at the preferred and fast speeds. The association between overall temporal symmetry and temporal swing symmetry is represented by a positive correlation (r⫽.94, df⫽52, P⬍.001). The association between overall temporal symmetry and temporal stance symmetry is represented by a negative correlation (r⫽⫺.77, df⫽52, P⬍.001) (fig 1). Mean values for spatial step symmetry at the preferred and fast velocities are summarized in table 1. Only 18 (33.3%) of the 54 participants exhibited a spatial step symmetry ratio outside the normative range of 0.9 to 1.1 (fig 2). It should be noted that 11 (61.1%) of these 18 subjects were classified as severely asymmetric temporally (classification described later). Spatial step symmetry ratio was not associated with overall temporal asymmetry (r⫽.03, df⫽52, P⫽.80) or preferred walking velocity (r⫽⫺.146, df⫽52, P⫽.292). In light of these results, the current study restricts its focus to the overall ratio of temporal asymmetry, because more participants exhibited temporal rather than spatial asymmetry. On the basis of the distribution of the overall temporal symmetry ratio we divided the group into 3 subgroups for the purposes of additional analysis: (1) normative (0.9 –1.1), (2) mild (1.1–1.5), and (3) severe (⬎1.5). This subdivision was based on the overall temporal symmetry at the preferred walking velocity. Although somewhat arbitrary, the cutoff value of 1.5 has some justification. Preliminary observations from ongoing work in our clinics have shown that physiotherapists can consistently detect the presence of temporal asymmetry among people with a symmetry index of 1.5 or greater. Values between 1.1 and 1.5 were more difficult to detect through observational approaches. Table 1 summarizes these 3 temporal symmetry categories (including demographics, mean velocity, symmetry ratios) that will be used to describe the data from this point forward.
3.50 Normative 3.00
Mild
2.50
Severe
2.00 1.50 1.00 0.50 0.00 0.00
20.00
40.00
60.00
80.00
100.00
120.00
140.00
160.00
Walking velocity (cm/s)
Fig 2. A between-subject comparison illustrating the negative correlation between preferred walking velocity and the overall temporal symmetry ratio at this speed (rⴝⴚ.583, dfⴝ52, P<.001). Each object represents 1 of the 54 participants and each shape represents a temporal symmetry category: severe asymmetry (triangles), mild asymmetry (squares) and normative symmetry (diamonds). Horizontal dashed lines represent the normative range for temporal symmetry (0.9 –1.1) based on a 95% CI around the mean temporal symmetry for 24 healthy control participants walking overground. Objects highlighted by a circle represent those subjects who also displayed spatial step asymmetry.
Relationship Between Asymmetry and Walking Velocity For between-subject comparisons, the mean preferred velocity for the entire group was 75.41⫾34.77cm/s. Mean fast velocity was 100.62⫾46.93cm/s (see table 1). There were 8 participants who could not increase their gait velocities on request. Three of these subjects had normative temporal symmetry and 5 exhibited severe temporal asymmetry at the preferred velocity. As mentioned above, in these cases the value of the preferred velocity was taken as the fastest gait velocity as well. The overall association between preferred walking velocity and overall temporal symmetry is represented by a statistically significant negative correlation (r⫽⫺.583, df⫽52, P⬍.001). Although there was a clear association between velocity and overall temporal symmetry, this was most strongly distinguished in those subjects with a much slower velocity. From visual inspection of the data it appears that those with a preferred velocity less than 60cm/s are more likely to exhibit severe overall temporal asymmetry (see fig 2). The mean overall symmetry of these slow walkers is 2.1⫾0.8 (range, 0.92– 4.52). All 4 subjects who wore an AFO during testing exhibited severe temporal asymmetry (range, 1.60 –2.57), and all but 1 of these subjects had a preferred gait velocity less than 60cm/s (range, 22.15– 86.53cm/s). Therefore, the 3 AFO users with gait speeds less than 60cm/s are nondescript within the severely asymmetric group in figure 2. The AFO user with a gait velocity of 86.53cm/s is distinct from the other participants with similar walking speeds (ie, 80 –95cm/s) in that that participant exhibited the largest overall temporal symmetry ratio (1.60), albeit not by a great amount. One-way ANOVA results showed a main effect of temporal symmetry group (normative, mild, severe) for preferred velocity (F⫽23.21, P⬍.001). Tukey analysis showed that the significant differences in mean preferred velocity were between the severe asymmetry group and both the normative symmetry and mild asymmetry groups. The mean preferred velocity was not significantly different between the mild asymmetry and normative symmetry groups. Arch Phys Med Rehabil Vol 89, February 2008
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GAIT ASYMMETRY AFTER STROKE, Patterson Table 2: The Effects of Increased Gait Velocity on Temporal Symmetry No Change
No Increase
Group
% of Group
Improved Symmetry Ratio Mean Change in Symmetry
% of Group
Worse Symmetry Ratio Mean Change in Symmetry
% of Group
% of Group
Whole (N⫽53) Normative symmetry (n⫽23) Mild asymmetry (n⫽12) Severe asymmetry (n⫽18)
50.9 34.8 66.7 61.1
10.05⫾13.39 4.40⫾2.57 7.78⫾6.38 15.82⫾19.15
32.1 47.8 33.3 11.1
8.24⫾10.51 5.57⫾5.00 3.73⫾3.43 31.99⫾13.96
1.9 4.3 0.0 0.0
15.1 13.0 0.0 27.8
NOTE. Values are mean ⫾ SD for the percentage change in symmetry (improved or worse) with increased velocity and the percentage of subjects within each group who exhibited the specified effect of increased gait velocity on temporal asymmetry as follows: improved, worsened, no change (indicates no change in symmetry with increased speed), and no increase (indicates those participants who were unable to increase the gait velocity above the preferred speed).
DISCUSSION The results illustrate that profound overall temporal asymmetry can be found in many stroke patients classified as independent ambulators. In this study, more than half (55.5%) of the participants exhibited temporal asymmetry. By comparison, fewer poststroke patients (33.3%) exhibited spatial step asymmetry. There is significant variation in temporal symmetry values within this functionally homogeneous group. Symmetry ratios ranged from within the normative range (0.9 –1.1) to Arch Phys Med Rehabil Vol 89, February 2008
A 5.00 4.50 4.00
Normative 3.50
Overall symmetry (ratio)
Relationship Between Asymmetry and Motor Impairment It is possible that the slow velocity and degree of asymmetry can be simply linked to the degree of limb impairment. If this were true then the index of limb impairment (CMSA) would be sufficient to express the expected variation in asymmetry and its relationship to velocity. Temporal symmetry appears partially related to motor impairment as measured by the CMSA. These significant negative correlations between the overall temporal symmetry ratio and CMSA scores for the foot (r⫽⫺.628, df⫽35, P⬍.001) and leg (r⫽⫺.644, df⫽35, P⬍.001) are depicted in figure 3. These relationships were particularly evident for subjects with preferred overall temporal symmetry values of 1.5 or higher (severe temporal asymmetry). One-way ANOVA results showed a main effect of temporal symmetry group (normative, mild, severe) for CMSA leg (F⫽12.42, P⬍.001) and foot scores (F⫽18.13, P⬍.001). Tukey analysis showed that the CMSA leg and foot scores were significantly different between the severe asymmetry group and both the normative symmetry and mild asymmetry groups. The CMSA leg and foot scores were not significantly different between the mild asymmetry and normative symmetry groups. Mean CMSA leg and foot scores are summarized in table 1.
severely asymmetric (4.52). This finding is consistent with that of Wall and Turnbull,10 who noted variation in asymmetry within a group of 25 “functionally ambulant” chronic stroke patients. Grouping persons with chronic stroke according to
Mild Severe
3.00 2.50 2.00 1.50 1.00 0.50 0.00 0
1
2
3
4
5
6
7
Foot impairment (CMSA foot score 0-7)
B 5.00 4.50 4.00 Overall symmetry (ratio)
Within-subject comparisons. In addition to the clear between-subject differences in walking velocity (associated with symmetry), there were also within-subject differences when comparing preferred and fast walking speeds. Twenty-seven (50.9%) of the 53 participants exhibited an improved temporal symmetry ratio (ie, moved closer to 1) at the fast velocity compared with the temporal symmetry ratio at the preferred velocity. Seventeen (32.1%) participants exhibited a worse temporal symmetry ratio or increased asymmetry (ie, moved further from 1) with increased walking velocity. The mean absolute percentage change in the overall temporal symmetry ratio for the entire group was 7.78%⫾11.69% when subjects walked faster. There appears to be between-subject and between-group differences in terms of the effect of increased walking velocity on overall temporal symmetry. These changes in symmetry are summarized in table 2.
3.50
Normative Mild Severe
3.00 2.50 2.00 1.50 1.00 0.50 0.00 0
1
2
3
4
5
6
7
Leg impairment (CMSA leg score 0-7)
Fig 3. Between-subject comparisons illustrating the negative correlation between the overall temporal symmetry ratio at the preferred gait speed and (A) CMSA foot score (rⴝ ⴚ.628, dfⴝ35, P<.001) and (B) CMSA leg score (rⴝ ⴚ.644, dfⴝ35, P<.001). Each shape represents a temporal symmetry category, severe asymmetry (triangles), mild asymmetry (squares), and normative symmetry (diamonds).
GAIT ASYMMETRY AFTER STROKE, Patterson
overall temporal symmetry at the preferred speed appears to have some merit in light of the complex relationship of temporal symmetry to motor impairment and gait velocity. Although use of CMSA scores and velocity alone can distinguish between people at the extremes of the spectrum (ie, fast and slow walkers, good and poor motor recovery), this approach does not distinguish among all poststroke ambulators, particularly those in the midrange (ie, velocity between 60 –100cm/s and CMSA scores between 4 – 6). With respect to the association between measures, spatial step asymmetry does not appear to correlate with temporal asymmetry or gait velocity. Although less prevalent, spatial step asymmetry appears more likely to occur in stroke survivors who exhibit severe temporal asymmetry compared with survivors who fall in the mild asymmetry or normative symmetry groups. Previous work has presented conflicting information regarding the relationship of gait speed and various measures of temporal symmetry.9,12 The current study clearly shows a relationship. However, it appears to be a nonlinear association in which greater degrees of asymmetry are associated with very slow walking speeds (⬍60cm/s). Such complexity of association may have influenced the ability to show such an association with smaller sample sizes or narrower ranges of patient abilities. There was a different association between temporal symmetry and walking velocity when comparing within individual participants. Those who are severely asymmetric appear more likely to exhibit improved temporal symmetry at their fast walking speeds. In contrast, those participants within the normative and mild asymmetry groups were equally likely to exhibit increased or decreased temporal asymmetry at a faster gait speed. It is not yet known whether these observed changes in temporal symmetry associated with increased gait speed are clinically significant. It is possible that the effect of increased velocity on temporal symmetry may depend on the specific underlying impairment causing the temporal asymmetry. The overall gait symmetry ratio in hemiplegic persons represents an increase in paretic swing duration and a decrease in paretic stance duration. Two possible impairments might lead to this pattern of asymmetry. First, an inability to generate sufficient muscle power to swing the paretic limb through quickly enough would result in prolonged swing duration for that limb.10 In this case, an increase in velocity would lead to a decrease in the amount of time available to swing the paretic limb through, thereby exacerbating the situation and resulting in a worsening of the temporal asymmetry. Alternatively, impaired balance that results in an inability to control the center of mass over the paretic limb could lead a person to shorten stance duration on this limb.10 In this situation, an increase in velocity would naturally lead to decreased time spent in the paretic stance, which may not affect the temporal symmetry ratio or could lead to an improvement in the symmetry ratio. Overall temporal symmetry also appears to be related to motor impairment of the leg and foot as measured by the CMSA. These findings correspond with previous studies using different measures of motor impairment (specifically, Brunnstrom stages and Fugl-Meyer Assessment).9,13 Similar to its relationship with velocity, the current study shows that the relationship of temporal symmetry and motor impairment is particularly evident for subjects who were severely asymmetric (ratios ⱖ1.5). Subjects with less motor impairment (CMSA leg scores of 6 and 7) may or may not exhibit temporally asymmetric gait. As mentioned above, although CMSA scores can distinguish among some stroke survivors, there are potentially important differences in poststroke gait not easily determined from
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CMSA scores alone. This is particularly true for those people in the middle range of motor function. It is possible that in the case of severe temporal asymmetry, gait function is heavily influenced by the degree of motor impairment, particularly in the leg. This may serve to limit a person’s capacity for forward progression during gait such that slow gait speed is an unavoidable consequence of severe temporal asymmetry. Those people exhibiting mild or moderate temporal asymmetries may have sufficient motor recovery in the lower limb to enable compensatory strategies to increase gait speed with varying degrees of success. In these cases, other factors beyond motor impairment—for example, dynamic balance control—may be more important determinants of walking competency. Clinical Relevance of Gait Asymmetry Although gait velocity is reflective of gait performance it does not, as identified by Olney et al,6 have “explicative capacity.” Used in isolation, gait speed neither assists in understanding the nature of poststroke gait deficits nor does it direct treatment.6 In addition, gait speed as a clinical outcome measure does not reflect components of a gait rehabilitation program related to training equal weight bearing and weight shifting. A measure of temporal gait symmetry included in quantitative gait analysis might better reflect this aspect of rehabilitation. It appears that the overall temporal symmetry ratio is superior to both swing and stance ratios as well as spatial symmetry ratios in discriminating among poststroke ambulators. Several studies have cited thresholds for gait velocity as a means of predicting ambulatory function. Holden et al26 identified 60cm/s, based on their review of the literature, as the minimum velocity needed for “a reasonable degree of functional independence,” defined as the ability to ambulate over all surfaces and all stairs. Perry et al27 cited 42cm/s as the cutoff for community ambulation. However, gait velocity when used alone is often insufficient in discriminating among poststroke ambulators. Perry27 noted that velocity alone failed to distinguish between the various levels of household ambulators. Taylor et al28 noted that gait velocity measured in the clinic was predictive of gait velocity in the community only for those with gait speeds greater than 80cm/s. The current results suggest that a measure of temporal symmetry may assist in further discrimination of poststroke ambulators, particularly those with gait speeds less than 60cm/s. Within this group, the overall temporal symmetry values cover a range of 3.6 (0.92– 4.52). In contrast, the range of overall temporal symmetry ratios for people with a preferred velocity greater than 60cm/s was only 0.65 (0.95–1.60). Specifically, classification of poststroke ambulators (particularly those who walk slower than 60cm/s) as exhibiting normative symmetry, mild asymmetry, or severe asymmetry may provide additional information regarding their gait performances. However, what needs to be determined now is the clinical relevance of these classifications. The functional implications of either immediate changes in temporal asymmetry with increased gait speed or long-term changes in temporal asymmetry with rehabilitation interventions are not yet known. Study Limitations This study focused on community-dwellers with chronic stroke, and therefore the results may not be generalizable to stroke patients in the acute stage or to people who need assistance for ambulation. In addition, the cross-sectional design of this study would not show changes in gait symmetry (and its relationship to velocity) that may occur within a person over Arch Phys Med Rehabil Vol 89, February 2008
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time. Finally, as noted previously, future work will need to link the degree of gait asymmetry to clinically relevant outcomes to better establish the clinical significance of such observations. CONCLUSIONS Roth et al12 suggested that a measure of temporal symmetry should be included in a comprehensive gait evaluation because they found that velocity did not correlate significantly with symmetry. We certainly agree with the view that gait symmetry ratio should be included as a measure of gait after stroke, even though the present study did show an association between symmetry and velocity. Although the specific nature of the association between symmetry and walking velocity is more complex than the linear model presently used, the current work emphasizes a potential link between disorders of control showed by asymmetry and the capacity to walk more quickly. Although velocity of walking certainly has implications for functional activities, there are many more potential consequences associated with gait asymmetry (challenges to dynamic balance control, increased risk of cumulative musculoskeletal injury, gait inefficiencies, limitations on walking speed). The findings of the present study and the importance of gait symmetry leads us to the view that gait symmetry should be the primary focus of poststroke assessment and that walking speed should serve as a complementary measure. It is our view that the ease of measurement, rather than clinical value, has led to the emphasis on measures such as gait velocity. New, clinically viable measurement approaches are emerging that can make the assessment of gait in rehabilitation settings more valuable to the clinician and patient. A clinical community more focused on important outcomes such as gait symmetry would further stimulate the development of simple cost-effective measurement solutions. References 1. Bohannon RW, Andrews AW, Smith MB. Rehabilitation goals of patients with hemiplegia. Int J Rehabil Res 1988;11:181-3. 2. Flansbjer U-B, Holmback AM, Downham D, Patten C, Lexell J. Reliability of gait performance tests in men and women with hemiparesis after stroke. J Rehabil Med 2005;37:75-82. 3. Macko RF, Ivey FM, Forrester LW, et al. Treadmill exercise rehabilitation improves ambulatory function and cardiovascular fitness in patients with chronic stroke. A randomized, controlled trial. Stroke 2005;36:2206-11. 4. Mizrahi J, Susak Z, Heller I, Najenson T. Variation of timedistance parameters of the stride as related to clinical gait improvement in hemiplegics. Scand J Rehabil Med 1982;14:133-40. 5. Lord SE, Halligan PW, Wade DT. Visual gait analysis: the development of a clinical assessment and scale. Clin Rehabil 1998; 12:107-19. 6. Olney SJ, Griffin MP, McBride ID. Temporal, kinematic and kinetic variables related to gait speed in subjects with hemiplegia: a regression approach. Phys Ther 1994;74:872-85. 7. Kim CM, Eng JJ. Symmetry in vertical ground reaction force is accompanied by symmetry in temporal but not distance variables of gait in persons with stroke. Gait Posture 2003;18:23-8. 8. Bohannon RW. Gait performance of hemiparetic stroke patients: selected variables. Arch Phys Med Rehabil 1987;68:777-81. 9. Brandstater ME, deBruin H, Gowland C, Clarke BM. Hemiplegic gait: analysis of temporal variables. Arch Phys Med Rehabil 1983;64:583-7.
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10. Wall JC, Turnbull GI. Gait asymmetries in residual hemiplegia. Arch Phys Med Rehabil 1986;67:550-3. 11. Griffin MP, Olney SJ, McBride ID. Role of symmetry in gait performance of stroke subjects with hemiplegia. Gait Posture 1995;3:132-42. 12. Roth EJ, Merbitz C, Mroczek K, Dugan SA, Suh WW. Hemiplegic gait: relationships between walking speed and other temporal parameters. Am J Phys Med Rehabil 1997;76:128-33. 13. Hsu AL, Tang PF, Jan MH. Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild to moderate stroke. Arch Phys Med Rehabil 2003;84:1185-93. 14. Davis BL, Ortolano M, Richards K, Redhed J, Kuznicki J, Sahgal V. Realtime visual feedback diminishes energy consumption of amputee subjects during treadmill locomotion. J Prosthet Orthot 2004;16:49-54. 15. Draper ER. A treadmill-based system for measuring symmetry of gait. Med Eng Phys 2000;22:215-22. 16. Platts MM, Rafferty D, Paul L. Metabolic cost of overground gait in younger stroke patients and healthy controls. Med Sci Sports Exerc 2006;38:1041-6. 17. Michael KM, Allen JK, Macko RF. Reduced ambulatory activity after stroke: the role of balance, gait and cardiovascular fitness. Arch Phys Med Rehabil 2005;86:1552-6. 18. Nolan L, Wit A, Dudzinski K, Lees A, Lake M, Wychowanski M. Adjustments in gait symmetry with walking speed in transfemoral and trans-tibial amputees. Gait Posture 2003;17:142-51. 19. Norvell DC, Czerniecki JM, Reiber GE, Maynard C, Pecoraro JA, Weiss NS. The prevalence of knee pain and symptomatic knee osteoarthritis among veteran traumatic amputees and nonamputees. Arch Phys Med Rehabil 2005;86:487-93. 20. Chen G, Patten C, Kothari DH, Zajac FE. Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds. Gait Posture 2005;22:51-6. 21. Lin P, Yang Y, Cheng S, Wang R. The relation between ankle impairments and gait velocity and symmetry in people with stroke. Arch Phys Med Rehabil 2006;87:562-8. 22. Gowland C, VanHullenaar S, Torresin W. Chedoke-McMaster Stroke Assessment: development, validation and administration manual. Hamilton: McMaster Univ; 1995. 23. Gowland C, Stratford P, Ward M, et al. Measuring physical impairment and disability with the Chedoke-McMaster stroke assessment. Stroke 1993;24:58-63. 24. Cohen E. Gait asymmetry and step to step variability post stroke [dissertation]. Toronto: Univ Toronto; 2004. 25. Patterson KK. Characteristics of independent ambulation in chronic stroke survivors. [dissertation]. Toronto: Univ Toronto; 2006. 26. Holden MK, Gill KM, Magliozzi MR. Gait assessment for neurologically impaired patients. Standards for outcome assessment. Phys Ther 1986;66:1530-9. 27. Perry J, Garrett M, Gronley JK, Mulroy SJ. Classification of walking handicap in the stroke population. Stroke 1995;26:982-9. 28. Taylor D, Stretton CM, Mudge S, Garrett N. Does clinic-measured gait speed differ from gait speed measured in the community in people with stroke? Clin Rehabil 2006;20:438-44. Suppliers a. CIR Systems, 1180 US Hwy 46, Parsippany, NJ 07054. b. Version 2003; Microsoft Corp, One Microsoft Way, Redmond, WA 98052. c. Version 9.1; SAS Institute Inc, 100 SAS Campus Dr, Cary, NC 27513.