Original article 311
Examination of spatiotemporal gait parameters during the 6-min walk in individuals with multiple sclerosis Michael J. Sociea, Robert W. Motlb and Jacob J. Sosnoffb This investigation examined spatiotemporal parameters of gait during the 6-min walk (6MW) in individuals with multiple sclerosis (MS) and in healthy controls. Eighteen individuals with MS [divided into those who were independently ambulatory (n = 10) and those who were ambulatory with assistance (n = 8)] and 10 healthy controls performed a 6MW while recording spatiotemporal gait parameters using a pressure-sensitive walkway. Parameters recorded were walking velocity, cadence, step length and width, step time, percent of the gait cycle in double support, and variability of step length and width, step time, and double support. The ambulatory with assistance MS group had a significantly greater reduction in walking velocity (P = 0.000) over the course of the 6MW, which coincided with a significantly greater increase in step time and double support (P = 0.029) than in the other groups. Only the ambulatory with assistance MS group showed an increase in step-time variability and double-support variability during the 6MW (P’s < 0.05). The novel results indicate that the reduction in velocity over prolonged walking occurs through a greater
change in the temporal parameters of gait in persons with MS who require assistance while walking. In addition, the increase in gait variability in the individuals with MS who require assistance while walking indicates that the control over walking further deteriorates over the course of the 6MW. International Journal of Rehabilitation Research 37:311–316 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins.
People with multiple sclerosis (MS) have gait impairment that adversely affects activities of daily living and quality of life (Zwibel, 2009; Larocca, 2011; Motl, 2013). This gait impairment is traditionally quantified with timed performance walk tests over relatively short distances, which yield an estimate of gait velocity (Bethoux and Bennett, 2011; Motl, 2013). The declines in gait velocity during these short walks correspond with decreases in both cadence and step length (Givon et al., 2009; Sosnoff et al., 2012).
performance during ambulatory capacity tests among individuals with MS. The identification of spatiotemporal parameters that change during walking capacity tests is important, because once identified, rehabilitation interventions can directly target these parameters in an effort to improve community ambulation (Cameron and Wagner, 2011).
In addition to declines in walking velocity, individuals with MS show a decline in walking capacity, as indexed by the distance walked in 2 or 6 min compared with agematched and sex-matched controls (Goldman et al., 2008; Gijbels et al., 2012). Assumed advantages of these capacity tests are that they more strongly relate to community ambulation compared with shorter tests (Motl et al., 2010; Weikert et al., 2012) and that they place greater demand on walking endurance, which can yield important observations with regard to gait changes associated with real-world ambulation. For instance, individuals with MS have been shown to decrease their walking speed over the course of the 6-min walk (6MW), and the amount of change scaled with disability level (Goldman et al., 2008). Currently, it is not clear what changes in the spatiotemporal parameters of gait underlie the decline in 0342-5282 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
International Journal of Rehabilitation Research 2014, 37:311–316 Keywords: fatigue, locomotion, mobility Departments of aMechanical Science and Engineering and bKinesiology and Community Health, University of Illinois at Urbana-Champaign, Champaign, Illinois, USA Correspondence to Jacob J. Sosnoff, PhD, Department of Kinesiology and Community Health, University of Illinois at Urbana-Champaign, 301 Freer Hall, 906 S. Goodwin Ave., Urbana, IL 61801, USA Tel: + 1 217 333 9472; fax: + 1 217 244 7322; e-mail: [email protected] Received 20 May 2014 Accepted 11 July 2014
There is growing evidence that variability in spatiotemporal parameters of walking provides unique information on walking and the health of the neuromuscular system (Hausdorff, 2005; Brach et al., 2007; Myers et al., 2010; Kaipust et al., 2012a). Recently, it has been demonstrated that individuals with MS who have minimal disability have elevated gait variability compared with healthy controls (Sosnoff et al., 2012) and that gait variability scales with disability (Socie et al., 2012a). There is also evidence that gait variability is associated with fall status in individuals with MS (Socie et al., 2012b). However, there is limited information on gait variability during walks of relatively long duration, such as the 6MW. The goal of the current investigation was to examine changes in spatiotemporal gait parameters, including measures of gait variability, during the 6MW in individuals with MS who vary by disability status compared with age-matched and sex-matched controls. DOI: 10.1097/MRR.0000000000000074
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312 International Journal of Rehabilitation Research 2014, Vol 37 No 4
Methods This study was approved by the Institutional Review Board of the University of Illinois at Urbana-Champaign. Upon arrival at the laboratory, all participants were informed of the experimental procedures and were asked to provide written informed consent.
also calculated. Parameters were averaged in 2-min segments, breaking the 6MW into three intervals to examine change over the course of the test. Two minutes was set as the interval duration so that all participants would have at least one pass over the GAITRite during each interval. Statistical analysis
Participants
The sample included 28 ambulatory communitydwelling individuals: 18 had a definite diagnosis of MS [14 female/four male, average age 47.1 years (SD 11.6 years)] and 10 were healthy controls [eight female/ two male, average age = 50.6 years (SD = 12.0 years)]. The MS group was further divided into subgroups on the basis of walking assistance (independently ambulatory, n = 10, and those who were ambulatory with assistance, n = 8). Six of those who utilized an assistive aid used unilateral support (e.g. canes), whereas the two other participants used bilateral support (e.g. walker). Inclusion criteria for the MS group included a diagnosis of MS, age between 18 and 64 years, and the ability to walk for 6 min (including the use of assistive devices such as canes and walkers). Inclusion criteria for controls were as follows: no history of neurological disorders and the ability to walk for 6 min without the use of assistive devices such as canes or walkers. Procedures
Participants with MS completed the Patient Determined Disease Steps (PDDS) scale, which provides a self-reported assessment of disability status. The PDDS scale ranges from 0 (no impairment) to 8 (bedridden; Rizzo et al., 2004; Marrie and Goldman, 2007). The PDDS scale is a valid and reliable assessment tool for disability status in MS (Learmonth et al., 2013). PDDS scores of 4 or higher indicate the use of an assistive device for ambulation. Participants with MS were divided into two groups on the basis of ambulatory status captured by PDDS: those who were independently ambulatory and ambulatory with assistance. On the basis of established 6MW procedures, participants were instructed to walk as far and as fast as safely possible in 6 min (Goldman et al., 2008). Notice was given to the participant as each minute passed and 3 s before the end of the test. The total distance walked was recorded with a measurement wheel (Stanley MW50; CST Berger, New Briton, Connecticut, USA). Participants walked up and down a 30-m corridor during the test, crossing the GAITRite (CIR Systems Inc., Haverton, Pennsylvania, USA) on each pass. Consequently, ∼ 15% of the total walk was sampled to measure spatiotemporal parameters of gait. Walking velocity, cadence, step time, step length, step width, and double-support percent of the gait cycle were measured throughout the 6MW using a 4.88 m GAITRite electronic walkway. The coefficient of variation (CV = SD/mean) of step time, step length, step width, and single-support and double-support time was
Statistical analysis was carried out using SPSS software version 21.0 (SPSS Inc., Chicago, Illinois, USA). Group differences in continuous demographic variables and 6MW performance were analyzed using one-way analysis of variance. Noncontinuous demographic variables were examined using χ2-tests. Group differences in spatiotemporal parameters were analyzed using mixed model analysis of variance, with group as the between-subject factor and interval as the within-subject factor. In addition, single-sample t-tests were used to determine whether the percentage change in each spatiotemporal parameter was significantly different from zero. Post-hoc analyses were used where appropriate for determining specific group and time differences. Significance was assumed at P less than 0.05.
Results Participant demographics
Table 1 lists participant demographics. There was no difference in age or sex between groups. Per design, individuals of the MS group who walked with assistance had greater PDDS scores than those who walked without assistance. Further, individuals of the MS group who walked with assistance had significantly longer disease duration than those who walked independently. Distance traveled during the 6-min walk
There was a significant difference between ambulation groups in the overall 6MW performance (F = 29.1, n = 0.00) as measured by total walking distance, with the independent ambulatory group traveling farther (522 m, SD = 104 m) than the ambulation with assistance group (237 m, SD = 127 m, P = 0.000). Both ambulation groups traveled significantly shorter distances compared with the healthy control group (607 m, SD = 87 m, P = 0.000, 0.042 assistance, independent groups, respectively). Spatiotemporal parameters
Average walking velocity, cadence, step length, step time, step width, and percent of gait cycle in doublesupport as a function of group and interval are reported in Table 2. Intraindividual variability in these parameters as a function of group and interval are reported in Table 3. Statistical analysis of average parameters revealed significant main effects of group and interval on walking velocity, cadence, step time, and step length (Table 4). Post-hoc analysis revealed that the ambulatory with assistance group walked slower with fewer shorter steps compared with the independent ambulatory and control
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Table 1
Group demographics
Group Independently ambulatory Ambulatory with assistance Healthy control
n
Age (SD)
No. of females/males
MS duration (SD)
PDDS (SD)
10 8 10
43.6 (9.1) 51.5 (13.4) 50.6 (12.0)
8/2 6/2 8/2
7.2 (5.1)a 14.3 (6.4)a NA
1.6 (1.5)a 4.5 (0.5)a NA
Significant difference was found between the two MS groups for years since diagnosis of MS. There were no differences in age or sex composition between the MS groups or between both MS groups and controls. MS, multiple sclerosis; PDDS, Patient Determined Disease Steps. a MS group differences. P < 0.05.
Table 2 Spatiotemporal gait parameters [mean (SD)] during each segment of the 6MW and the mean percentage change in each parameter from first the 2-min interval to the last 2-min interval are shown for each group Spatiotemporal parameters Walking velocity (cm/s)
Cadence (steps/min)
Step length (cm)
Double support (%)
Step time (s)
Step width (cm)
Ambulation group Control IA AA Control IA AA Control IA AA Control IA AA Control IA AA Control IA AA
Minutes 1–2 173.7 150.0 68.7 128.7 121.3 88.0 81.0 73.9 46.2 24.4 26.9 39.3 0.47 0.50 0.72 9.9 10.8 12.7
(24.8) (30.3)b,c (36.2)b,c (11.7) (11.4)b (19.8)b,c (8.6) (8.9)b (17.0)b,c (4.7) (6.6)b (24.5)b,c (0.04) (.05) (0.17)b,c (1.4) (2.0) (5.1)c
Minutes 3–4 169.7 147.4 65.6 126.6 120.2 85.9 80.5 73.1 44.0 24.5 27.3 41.3 0.48 0.50 0.74 9.6 11.0 11.6
(23.5) (30.2)b (37.2)b,c (12.3) (11.5)b (21.8)b,c (8.3) (9.1)b (17.3)b,c (4.9) (7.1)b (33.0)b,c (0.05) (0.05) (0.20)b,c (1.3) (2.2) (4.6)c
Minutes 5–6 169.5 147.8 65.4 126.6 120.2 84.7 80.4 73.4 44.6 24.6 27.1 40.9 0.48 0.50 0.76 9.6 10.8 12.1
(24.9) (31.3)b (36.7)b,c (13.1) (12.1)b (23.2)b,c (9.0) (9.1)b (16.3)b,c (4.7) (7.3)b (34.0)b,c (0.05) (0.05) (0.23)b,c (1.4) (2.3) (4.5)c
Percentage change − 2.4a − 1.6b,a − 6.7b,c,a − 1.6 − 1.0b,a − 4.8b,a − 0.7 − 0.7 − 2.9 1.1 0.4 3.7 2.0 0.0 5.6b,c,a − 3.1 0.4 − 1.3
AA, ambulatory with assistance; IA, independently ambulatory; MS, multiple sclerosis; 6MW, 6-min walk. a Different from zero. b MS group differences. c Different from controls. P < 0.05.
Table 3 Variability of spatiotemporal gait parameters during each segment of the 6MW and the mean ercentage change in each parameter from the first 2-min interval to the last 2-min interval as a function of group Parameters Step-time CV (%)
Step-length CV (%)
Step-width CV (%)
Double-support CV (%)
Ambulation group Control IA AA Control IA AA Control IA AA Control IA AA
Minutes 1–2
Minutes 3–4
Minutes 5–6
2.7 2.7 4.7 1.9 2.3 8.9 21.1 20.1 17.1 4.0 4.7 5.2
2.1 2.8 11.0 1.8 2.3 11.6 20.5 17.6 15.2 3.8 4.3 12.5
2.1 2.6 9.4 1.8 2.2 12.8 18.7 19.7 30.8 3.5 4.3 9.4
(1.1) (1.1) (1.7)a,b (0.9) (1.0) (5.5)a,b (10.5) (7.8) (10.5) (1.1) (2.2) (1.6)
(0.5) (1.2) (6.5)a,b (0.5) (1.1) (7.7)a,b (6.6) (6.1) (9.9) (0.7) (1.2) (7.7)
(0.7) (1.1) (6.8)a,b (0.5) (0.9) (13.5)a,b (7.1) (9.2) (28.5) (1.1) (1.9) (5.0)
Percentage change 0 − 3.7 100c − 5.2 − 4.5 43.8c − 11.3 − 2.3 80.1c − 12.5 − 9.3 80.8c
AA, Ambulatory with assistance; CV, coefficient of variation; IA, Independently ambulatory; MS, multiple sclerosis; 6MW, 6-min walk. a MS group differences. b Different from controls. c Different from zero. P < 0.05.
groups. Overall, walking in the first 2-min interval was faster, with more (i.e. greater cadence) and longer steps than in the middle and last 2-min intervals. There was a significant interaction of group and interval on step time and percentage of gait cycle with two feet on
the ground. The interaction resulted from the ambulatory with assistance group increasing step time and percentage of gait cycle with two feet on the ground over the duration of the 6MW while the other groups did not statistically change. There were no main effects or interactions for step width.
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Analysis of variance table for mean and variability spatiotemporal parameters
Table 4
Parameters
Group F(2,25)
Time F(2,50)
Group by time F(4,50)
29.1* 28.1* 17.8* 22.7* 2.2 13.5* 17.7* 12.8* 0.1 16.8* 11.5*
− 16.7* 10.3* 8.7* 0.6 8.0* 12.2* 1.0 2.0 5.3* 6.3*
− 0.7 1.1 1.7 0.4 3.1* 4.2* 1.1 2.4 6.7* 7.5*
6-min walk distance Walking velocity Cadence Step length Step width Step time Double support Step-length CV Step-width CV Step-time CV Double-support CV CV, coefficient of variation. *P < 0.05.
Statistical analysis of intraindividual variability revealed a significant main effect of group on step-time variability, step length, and double-support variability (Table 4). There was a significant effect of interval on step time and double-support variability. There was also a significant interaction of group and interval on step-time variability and double-support variability. The group effect resulted from the ambulatory with assistance group having greater step time, step length, and double-support variability compared with the other groups. The interval effect resulted from the gait variability in the middle interval being greater than in the first and last intervals. The interaction between group and interval resulted from only the ambulatory with assistance group increasing in step-time variability and double-support variability over the course of the 6MW.
Discussion Walking impairments in individuals with MS are well documented (Givon et al., 2009; Bethoux and Bennett, 2011; Sosnoff et al., 2012; Motl, 2013). The vast majority of research has examined spatiotemporal parameters of walking during short-distance walks (e.g. 10 m). There has been a call to include longer walks that examine walking capacity in the assessment of walking in individuals with MS (Bethoux and Bennett, 2011; Gijbels et al., 2011, 2012; Sosnoff et al., 2012). An assumed advantage of these capacity tests is that they are more strongly related to community ambulation than shorter tests (Motl et al., 2010; Weikert et al., 2012) and better stress the musculoskeletal system during walking. The unique aspect of this investigation was the quantification of spatiotemporal gait parameters and variability of these parameters during the 6MW in individuals with MS both with and without impaired gait, as well as in healthy controls without MS. Overall, all participants were found to decrease their walking velocity over the course of the 6MW, with the greatest decline in velocity in the ambulatory with assistance MS group. The decline in velocity in the ambulatory with assistance group was coupled with a change in the temporal parameters of gait
(cadence, step time, double support) and an increase in gait variability. These observations have important implications in understanding gait impairment in MS during longer duration walks and perhaps communitybased ambulation. Specifically, the observations may suggest that rehabilitation programs seeking to improve walking capacity in persons who require assistance while walking should focus on the timing of gait and not the spatial aspects. A caveat to this proposal is the interdependence between temporal and spatial aspects of gait. Further work examining this issue is warranted. In addition to novel results pertaining to spatiotemporal gait parameters during the 6MW, we replicated differences between MS groups in overall 6MW performance. Both MS groups traveled significantly shorter distances than healthy controls. These results are congruent with a previous report (Goldman et al., 2008), which found a decrease in 6MW distance in more impaired individuals with MS compared with individuals with less disability. However, that report did not report differences between mild MS and controls, which we have shown in this investigation. The gait in the ambulatory with assistance group was distinct from that in healthy controls throughout the 6MW in all the spatiotemporal parameters examined. In contrast, individuals with MS who were independently ambulatory did not show a significantly different gait from controls. This is in contrast to previous reports indicating that individuals with MS who have minimal disability show altered gait in comparison with age, sex, height, and weight matched controls (Sosnoff et al., 2012). There are at least two potential reasons explaining this discrepancy. First, the instructions provided to the participants and task performed are distinct across investigations. Within the current investigation, participants were told to walk as fast and as far as possible for 6 min, whereas in the previous report individuals walked at a self-selected comfortable pace (Sosnoff et al., 2012). In support of this possibility is a recent report documenting that instructions manipulating walking speed cause significant changes in gait in individuals with MS (Feys et al., 2013). Alternatively, it is possible that the current investigation lacked statistical power to distinguish between individuals with MS with mild gait impairment and healthy controls. The independently ambulating group was not significantly different from controls for all spatiotemporal gait parameters, with the exception of velocity in the first 2 min of the test. The presence of a significant difference between independently ambulatory individuals with MS and controls in velocity in only the first 2 min of the 6MW illustrates potential differences between the 6MW and 2-min walk tests. It has been suggested that the final 4 min of the 6MW provide redundant information to the
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Examination of spatiotemporal gait parameters Socie et al. 315
2-min walk test (Gijbels et al., 2011). However, the changes in walking behavior over the course of the 6MW in this investigation do not support that assertion. The potential differences between the 6MW and 2-min walk tests and appropriate use of them merits further investigation. Individuals with MS who required assistance while walking had greater step length and time variability than those who did not require assistance. These observations are congruent with an investigation of 88 ambulatory individuals with MS, which documented that clinical disability as indexed by the expanded disability status scale was positively correlated with step-length variability (Socie et al., 2012a). A potentially important observation was that gait variability increased over the course of the 6MW in individuals with MS who required assistance while walking. Indeed, changes in gait variability observed were up to 10 times larger than those seen for mean spatiotemporal parameters. This is congruent with the theoretical notion that measures of variability are sensitive to impaired neuromuscular function (Newell et al., 2006). Increases in gait variability are indicative of impairment in control of gait (Hausdorff, 2005; Balasubramanian et al., 2009; Kaipust et al., 2012a). The increased gait variability during the course of the 6MW indicates that individuals with MS who require assistance while walking have a further decline in the control of walking during the 6MW. Various factors such as muscle strength (Shin et al., 2012) and neuromotor noise (Roos and Dingwell, 2010) might contribute to elevated gait variability in clinical populations. The mechanism underlying the elevated gait variability in individuals with MS remains to be elucidated (Socie and Sosnoff, 2013). In addition to the theoretical importance of the observed increase in step length and time variability, the alterations in variability have practical implications. Gait variability has been experimentally associated with increased energetic cost of walking (O’Connor et al. 2012). Perhaps the elevated energetic cost of walking observed in individuals with MS is due in part to greater gait variability. Extreme gait variability has been linked to falls in clinical populations including individuals with MS (Hausdorff, 2005; Callisaya et al., 2011; Socie et al., 2012b). This raises that possibility that individuals utilizing an assistive device while walking are at an increased risk for falls during the later stages of the 6MW. There was no significant change in other gait parameters related to stability (i.e. double support or step width). Despite the novel observations, this investigation has a few limitations. Perhaps the largest limitation is that spatiotemporal parameters were sampled during ∼15% of the test instead of the entire 6MW and the sample size was relatively small. Another potential limitation is the possibility that participants changed their gait as they crossed the GAITRite mat. This phenomenon was not visually apparent during testing, and the overall velocity
(distance walked divided by 6 min) closely resembled velocity calculated by the GAITRite software. Regardless, use of different technology, for example, accelerometry (Motl et al., 2012; Spain et al., 2012), could offer the means to continuously measure parameters while removing the potential for changes in gait due to the presence of the GAITRite walkway. In summary, the novel results of this investigation indicate that the reduction in walking velocity during the 6MW in individuals with MS who require assistance while walking occurs mainly through a change in the temporal properties of gait. This indirectly suggests that rehabilitation approaches targeting gait timing could result in improvements in 6MW performance. In addition, the marked increase in gait variability in the individuals with MS who require assistance while walking indicates that the control of walking further deteriorates over the course of the 6MW test.
Acknowledgements The authors thank M.K. Boes for assistance with data collection and the staff of the Illinois Simulator Laboratory at the University of Illinois at Urbana-Champaign. Conflicts of interest
There are no conflicts of interest.
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Examination of spatiotemporal gait parameters during the 6-min walk in individuals with multiple sclerosis Michael J. Sociea, Robert W. Motlb and Jacob J. Sosnoffb This investigation examined spatiotemporal parameters of gait during the 6-min walk (6MW) in individuals with multiple sclerosis (MS) and in healthy controls. Eighteen individuals with MS [divided into those who were independently ambulatory (n = 10) and those who were ambulatory with assistance (n = 8)] and 10 healthy controls performed a 6MW while recording spatiotemporal gait parameters using a pressure-sensitive walkway. Parameters recorded were walking velocity, cadence, step length and width, step time, percent of the gait cycle in double support, and variability of step length and width, step time, and double support. The ambulatory with assistance MS group had a significantly greater reduction in walking velocity (P = 0.000) over the course of the 6MW, which coincided with a significantly greater increase in step time and double support (P = 0.029) than in the other groups. Only the ambulatory with assistance MS group showed an increase in step-time variability and double-support variability during the 6MW (P’s < 0.05). The novel results indicate that the reduction in velocity over prolonged walking occurs through a greater
change in the temporal parameters of gait in persons with MS who require assistance while walking. In addition, the increase in gait variability in the individuals with MS who require assistance while walking indicates that the control over walking further deteriorates over the course of the 6MW. International Journal of Rehabilitation Research 37:311–316 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins.
People with multiple sclerosis (MS) have gait impairment that adversely affects activities of daily living and quality of life (Zwibel, 2009; Larocca, 2011; Motl, 2013). This gait impairment is traditionally quantified with timed performance walk tests over relatively short distances, which yield an estimate of gait velocity (Bethoux and Bennett, 2011; Motl, 2013). The declines in gait velocity during these short walks correspond with decreases in both cadence and step length (Givon et al., 2009; Sosnoff et al., 2012).
performance during ambulatory capacity tests among individuals with MS. The identification of spatiotemporal parameters that change during walking capacity tests is important, because once identified, rehabilitation interventions can directly target these parameters in an effort to improve community ambulation (Cameron and Wagner, 2011).
In addition to declines in walking velocity, individuals with MS show a decline in walking capacity, as indexed by the distance walked in 2 or 6 min compared with agematched and sex-matched controls (Goldman et al., 2008; Gijbels et al., 2012). Assumed advantages of these capacity tests are that they more strongly relate to community ambulation compared with shorter tests (Motl et al., 2010; Weikert et al., 2012) and that they place greater demand on walking endurance, which can yield important observations with regard to gait changes associated with real-world ambulation. For instance, individuals with MS have been shown to decrease their walking speed over the course of the 6-min walk (6MW), and the amount of change scaled with disability level (Goldman et al., 2008). Currently, it is not clear what changes in the spatiotemporal parameters of gait underlie the decline in 0342-5282 © 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
International Journal of Rehabilitation Research 2014, 37:311–316 Keywords: fatigue, locomotion, mobility Departments of aMechanical Science and Engineering and bKinesiology and Community Health, University of Illinois at Urbana-Champaign, Champaign, Illinois, USA Correspondence to Jacob J. Sosnoff, PhD, Department of Kinesiology and Community Health, University of Illinois at Urbana-Champaign, 301 Freer Hall, 906 S. Goodwin Ave., Urbana, IL 61801, USA Tel: + 1 217 333 9472; fax: + 1 217 244 7322; e-mail: [email protected] Received 20 May 2014 Accepted 11 July 2014
There is growing evidence that variability in spatiotemporal parameters of walking provides unique information on walking and the health of the neuromuscular system (Hausdorff, 2005; Brach et al., 2007; Myers et al., 2010; Kaipust et al., 2012a). Recently, it has been demonstrated that individuals with MS who have minimal disability have elevated gait variability compared with healthy controls (Sosnoff et al., 2012) and that gait variability scales with disability (Socie et al., 2012a). There is also evidence that gait variability is associated with fall status in individuals with MS (Socie et al., 2012b). However, there is limited information on gait variability during walks of relatively long duration, such as the 6MW. The goal of the current investigation was to examine changes in spatiotemporal gait parameters, including measures of gait variability, during the 6MW in individuals with MS who vary by disability status compared with age-matched and sex-matched controls. DOI: 10.1097/MRR.0000000000000074
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Methods This study was approved by the Institutional Review Board of the University of Illinois at Urbana-Champaign. Upon arrival at the laboratory, all participants were informed of the experimental procedures and were asked to provide written informed consent.
also calculated. Parameters were averaged in 2-min segments, breaking the 6MW into three intervals to examine change over the course of the test. Two minutes was set as the interval duration so that all participants would have at least one pass over the GAITRite during each interval. Statistical analysis
Participants
The sample included 28 ambulatory communitydwelling individuals: 18 had a definite diagnosis of MS [14 female/four male, average age 47.1 years (SD 11.6 years)] and 10 were healthy controls [eight female/ two male, average age = 50.6 years (SD = 12.0 years)]. The MS group was further divided into subgroups on the basis of walking assistance (independently ambulatory, n = 10, and those who were ambulatory with assistance, n = 8). Six of those who utilized an assistive aid used unilateral support (e.g. canes), whereas the two other participants used bilateral support (e.g. walker). Inclusion criteria for the MS group included a diagnosis of MS, age between 18 and 64 years, and the ability to walk for 6 min (including the use of assistive devices such as canes and walkers). Inclusion criteria for controls were as follows: no history of neurological disorders and the ability to walk for 6 min without the use of assistive devices such as canes or walkers. Procedures
Participants with MS completed the Patient Determined Disease Steps (PDDS) scale, which provides a self-reported assessment of disability status. The PDDS scale ranges from 0 (no impairment) to 8 (bedridden; Rizzo et al., 2004; Marrie and Goldman, 2007). The PDDS scale is a valid and reliable assessment tool for disability status in MS (Learmonth et al., 2013). PDDS scores of 4 or higher indicate the use of an assistive device for ambulation. Participants with MS were divided into two groups on the basis of ambulatory status captured by PDDS: those who were independently ambulatory and ambulatory with assistance. On the basis of established 6MW procedures, participants were instructed to walk as far and as fast as safely possible in 6 min (Goldman et al., 2008). Notice was given to the participant as each minute passed and 3 s before the end of the test. The total distance walked was recorded with a measurement wheel (Stanley MW50; CST Berger, New Briton, Connecticut, USA). Participants walked up and down a 30-m corridor during the test, crossing the GAITRite (CIR Systems Inc., Haverton, Pennsylvania, USA) on each pass. Consequently, ∼ 15% of the total walk was sampled to measure spatiotemporal parameters of gait. Walking velocity, cadence, step time, step length, step width, and double-support percent of the gait cycle were measured throughout the 6MW using a 4.88 m GAITRite electronic walkway. The coefficient of variation (CV = SD/mean) of step time, step length, step width, and single-support and double-support time was
Statistical analysis was carried out using SPSS software version 21.0 (SPSS Inc., Chicago, Illinois, USA). Group differences in continuous demographic variables and 6MW performance were analyzed using one-way analysis of variance. Noncontinuous demographic variables were examined using χ2-tests. Group differences in spatiotemporal parameters were analyzed using mixed model analysis of variance, with group as the between-subject factor and interval as the within-subject factor. In addition, single-sample t-tests were used to determine whether the percentage change in each spatiotemporal parameter was significantly different from zero. Post-hoc analyses were used where appropriate for determining specific group and time differences. Significance was assumed at P less than 0.05.
Results Participant demographics
Table 1 lists participant demographics. There was no difference in age or sex between groups. Per design, individuals of the MS group who walked with assistance had greater PDDS scores than those who walked without assistance. Further, individuals of the MS group who walked with assistance had significantly longer disease duration than those who walked independently. Distance traveled during the 6-min walk
There was a significant difference between ambulation groups in the overall 6MW performance (F = 29.1, n = 0.00) as measured by total walking distance, with the independent ambulatory group traveling farther (522 m, SD = 104 m) than the ambulation with assistance group (237 m, SD = 127 m, P = 0.000). Both ambulation groups traveled significantly shorter distances compared with the healthy control group (607 m, SD = 87 m, P = 0.000, 0.042 assistance, independent groups, respectively). Spatiotemporal parameters
Average walking velocity, cadence, step length, step time, step width, and percent of gait cycle in doublesupport as a function of group and interval are reported in Table 2. Intraindividual variability in these parameters as a function of group and interval are reported in Table 3. Statistical analysis of average parameters revealed significant main effects of group and interval on walking velocity, cadence, step time, and step length (Table 4). Post-hoc analysis revealed that the ambulatory with assistance group walked slower with fewer shorter steps compared with the independent ambulatory and control
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Examination of spatiotemporal gait parameters Socie et al. 313
Table 1
Group demographics
Group Independently ambulatory Ambulatory with assistance Healthy control
n
Age (SD)
No. of females/males
MS duration (SD)
PDDS (SD)
10 8 10
43.6 (9.1) 51.5 (13.4) 50.6 (12.0)
8/2 6/2 8/2
7.2 (5.1)a 14.3 (6.4)a NA
1.6 (1.5)a 4.5 (0.5)a NA
Significant difference was found between the two MS groups for years since diagnosis of MS. There were no differences in age or sex composition between the MS groups or between both MS groups and controls. MS, multiple sclerosis; PDDS, Patient Determined Disease Steps. a MS group differences. P < 0.05.
Table 2 Spatiotemporal gait parameters [mean (SD)] during each segment of the 6MW and the mean percentage change in each parameter from first the 2-min interval to the last 2-min interval are shown for each group Spatiotemporal parameters Walking velocity (cm/s)
Cadence (steps/min)
Step length (cm)
Double support (%)
Step time (s)
Step width (cm)
Ambulation group Control IA AA Control IA AA Control IA AA Control IA AA Control IA AA Control IA AA
Minutes 1–2 173.7 150.0 68.7 128.7 121.3 88.0 81.0 73.9 46.2 24.4 26.9 39.3 0.47 0.50 0.72 9.9 10.8 12.7
(24.8) (30.3)b,c (36.2)b,c (11.7) (11.4)b (19.8)b,c (8.6) (8.9)b (17.0)b,c (4.7) (6.6)b (24.5)b,c (0.04) (.05) (0.17)b,c (1.4) (2.0) (5.1)c
Minutes 3–4 169.7 147.4 65.6 126.6 120.2 85.9 80.5 73.1 44.0 24.5 27.3 41.3 0.48 0.50 0.74 9.6 11.0 11.6
(23.5) (30.2)b (37.2)b,c (12.3) (11.5)b (21.8)b,c (8.3) (9.1)b (17.3)b,c (4.9) (7.1)b (33.0)b,c (0.05) (0.05) (0.20)b,c (1.3) (2.2) (4.6)c
Minutes 5–6 169.5 147.8 65.4 126.6 120.2 84.7 80.4 73.4 44.6 24.6 27.1 40.9 0.48 0.50 0.76 9.6 10.8 12.1
(24.9) (31.3)b (36.7)b,c (13.1) (12.1)b (23.2)b,c (9.0) (9.1)b (16.3)b,c (4.7) (7.3)b (34.0)b,c (0.05) (0.05) (0.23)b,c (1.4) (2.3) (4.5)c
Percentage change − 2.4a − 1.6b,a − 6.7b,c,a − 1.6 − 1.0b,a − 4.8b,a − 0.7 − 0.7 − 2.9 1.1 0.4 3.7 2.0 0.0 5.6b,c,a − 3.1 0.4 − 1.3
AA, ambulatory with assistance; IA, independently ambulatory; MS, multiple sclerosis; 6MW, 6-min walk. a Different from zero. b MS group differences. c Different from controls. P < 0.05.
Table 3 Variability of spatiotemporal gait parameters during each segment of the 6MW and the mean ercentage change in each parameter from the first 2-min interval to the last 2-min interval as a function of group Parameters Step-time CV (%)
Step-length CV (%)
Step-width CV (%)
Double-support CV (%)
Ambulation group Control IA AA Control IA AA Control IA AA Control IA AA
Minutes 1–2
Minutes 3–4
Minutes 5–6
2.7 2.7 4.7 1.9 2.3 8.9 21.1 20.1 17.1 4.0 4.7 5.2
2.1 2.8 11.0 1.8 2.3 11.6 20.5 17.6 15.2 3.8 4.3 12.5
2.1 2.6 9.4 1.8 2.2 12.8 18.7 19.7 30.8 3.5 4.3 9.4
(1.1) (1.1) (1.7)a,b (0.9) (1.0) (5.5)a,b (10.5) (7.8) (10.5) (1.1) (2.2) (1.6)
(0.5) (1.2) (6.5)a,b (0.5) (1.1) (7.7)a,b (6.6) (6.1) (9.9) (0.7) (1.2) (7.7)
(0.7) (1.1) (6.8)a,b (0.5) (0.9) (13.5)a,b (7.1) (9.2) (28.5) (1.1) (1.9) (5.0)
Percentage change 0 − 3.7 100c − 5.2 − 4.5 43.8c − 11.3 − 2.3 80.1c − 12.5 − 9.3 80.8c
AA, Ambulatory with assistance; CV, coefficient of variation; IA, Independently ambulatory; MS, multiple sclerosis; 6MW, 6-min walk. a MS group differences. b Different from controls. c Different from zero. P < 0.05.
groups. Overall, walking in the first 2-min interval was faster, with more (i.e. greater cadence) and longer steps than in the middle and last 2-min intervals. There was a significant interaction of group and interval on step time and percentage of gait cycle with two feet on
the ground. The interaction resulted from the ambulatory with assistance group increasing step time and percentage of gait cycle with two feet on the ground over the duration of the 6MW while the other groups did not statistically change. There were no main effects or interactions for step width.
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Analysis of variance table for mean and variability spatiotemporal parameters
Table 4
Parameters
Group F(2,25)
Time F(2,50)
Group by time F(4,50)
29.1* 28.1* 17.8* 22.7* 2.2 13.5* 17.7* 12.8* 0.1 16.8* 11.5*
− 16.7* 10.3* 8.7* 0.6 8.0* 12.2* 1.0 2.0 5.3* 6.3*
− 0.7 1.1 1.7 0.4 3.1* 4.2* 1.1 2.4 6.7* 7.5*
6-min walk distance Walking velocity Cadence Step length Step width Step time Double support Step-length CV Step-width CV Step-time CV Double-support CV CV, coefficient of variation. *P < 0.05.
Statistical analysis of intraindividual variability revealed a significant main effect of group on step-time variability, step length, and double-support variability (Table 4). There was a significant effect of interval on step time and double-support variability. There was also a significant interaction of group and interval on step-time variability and double-support variability. The group effect resulted from the ambulatory with assistance group having greater step time, step length, and double-support variability compared with the other groups. The interval effect resulted from the gait variability in the middle interval being greater than in the first and last intervals. The interaction between group and interval resulted from only the ambulatory with assistance group increasing in step-time variability and double-support variability over the course of the 6MW.
Discussion Walking impairments in individuals with MS are well documented (Givon et al., 2009; Bethoux and Bennett, 2011; Sosnoff et al., 2012; Motl, 2013). The vast majority of research has examined spatiotemporal parameters of walking during short-distance walks (e.g. 10 m). There has been a call to include longer walks that examine walking capacity in the assessment of walking in individuals with MS (Bethoux and Bennett, 2011; Gijbels et al., 2011, 2012; Sosnoff et al., 2012). An assumed advantage of these capacity tests is that they are more strongly related to community ambulation than shorter tests (Motl et al., 2010; Weikert et al., 2012) and better stress the musculoskeletal system during walking. The unique aspect of this investigation was the quantification of spatiotemporal gait parameters and variability of these parameters during the 6MW in individuals with MS both with and without impaired gait, as well as in healthy controls without MS. Overall, all participants were found to decrease their walking velocity over the course of the 6MW, with the greatest decline in velocity in the ambulatory with assistance MS group. The decline in velocity in the ambulatory with assistance group was coupled with a change in the temporal parameters of gait
(cadence, step time, double support) and an increase in gait variability. These observations have important implications in understanding gait impairment in MS during longer duration walks and perhaps communitybased ambulation. Specifically, the observations may suggest that rehabilitation programs seeking to improve walking capacity in persons who require assistance while walking should focus on the timing of gait and not the spatial aspects. A caveat to this proposal is the interdependence between temporal and spatial aspects of gait. Further work examining this issue is warranted. In addition to novel results pertaining to spatiotemporal gait parameters during the 6MW, we replicated differences between MS groups in overall 6MW performance. Both MS groups traveled significantly shorter distances than healthy controls. These results are congruent with a previous report (Goldman et al., 2008), which found a decrease in 6MW distance in more impaired individuals with MS compared with individuals with less disability. However, that report did not report differences between mild MS and controls, which we have shown in this investigation. The gait in the ambulatory with assistance group was distinct from that in healthy controls throughout the 6MW in all the spatiotemporal parameters examined. In contrast, individuals with MS who were independently ambulatory did not show a significantly different gait from controls. This is in contrast to previous reports indicating that individuals with MS who have minimal disability show altered gait in comparison with age, sex, height, and weight matched controls (Sosnoff et al., 2012). There are at least two potential reasons explaining this discrepancy. First, the instructions provided to the participants and task performed are distinct across investigations. Within the current investigation, participants were told to walk as fast and as far as possible for 6 min, whereas in the previous report individuals walked at a self-selected comfortable pace (Sosnoff et al., 2012). In support of this possibility is a recent report documenting that instructions manipulating walking speed cause significant changes in gait in individuals with MS (Feys et al., 2013). Alternatively, it is possible that the current investigation lacked statistical power to distinguish between individuals with MS with mild gait impairment and healthy controls. The independently ambulating group was not significantly different from controls for all spatiotemporal gait parameters, with the exception of velocity in the first 2 min of the test. The presence of a significant difference between independently ambulatory individuals with MS and controls in velocity in only the first 2 min of the 6MW illustrates potential differences between the 6MW and 2-min walk tests. It has been suggested that the final 4 min of the 6MW provide redundant information to the
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Examination of spatiotemporal gait parameters Socie et al. 315
2-min walk test (Gijbels et al., 2011). However, the changes in walking behavior over the course of the 6MW in this investigation do not support that assertion. The potential differences between the 6MW and 2-min walk tests and appropriate use of them merits further investigation. Individuals with MS who required assistance while walking had greater step length and time variability than those who did not require assistance. These observations are congruent with an investigation of 88 ambulatory individuals with MS, which documented that clinical disability as indexed by the expanded disability status scale was positively correlated with step-length variability (Socie et al., 2012a). A potentially important observation was that gait variability increased over the course of the 6MW in individuals with MS who required assistance while walking. Indeed, changes in gait variability observed were up to 10 times larger than those seen for mean spatiotemporal parameters. This is congruent with the theoretical notion that measures of variability are sensitive to impaired neuromuscular function (Newell et al., 2006). Increases in gait variability are indicative of impairment in control of gait (Hausdorff, 2005; Balasubramanian et al., 2009; Kaipust et al., 2012a). The increased gait variability during the course of the 6MW indicates that individuals with MS who require assistance while walking have a further decline in the control of walking during the 6MW. Various factors such as muscle strength (Shin et al., 2012) and neuromotor noise (Roos and Dingwell, 2010) might contribute to elevated gait variability in clinical populations. The mechanism underlying the elevated gait variability in individuals with MS remains to be elucidated (Socie and Sosnoff, 2013). In addition to the theoretical importance of the observed increase in step length and time variability, the alterations in variability have practical implications. Gait variability has been experimentally associated with increased energetic cost of walking (O’Connor et al. 2012). Perhaps the elevated energetic cost of walking observed in individuals with MS is due in part to greater gait variability. Extreme gait variability has been linked to falls in clinical populations including individuals with MS (Hausdorff, 2005; Callisaya et al., 2011; Socie et al., 2012b). This raises that possibility that individuals utilizing an assistive device while walking are at an increased risk for falls during the later stages of the 6MW. There was no significant change in other gait parameters related to stability (i.e. double support or step width). Despite the novel observations, this investigation has a few limitations. Perhaps the largest limitation is that spatiotemporal parameters were sampled during ∼15% of the test instead of the entire 6MW and the sample size was relatively small. Another potential limitation is the possibility that participants changed their gait as they crossed the GAITRite mat. This phenomenon was not visually apparent during testing, and the overall velocity
(distance walked divided by 6 min) closely resembled velocity calculated by the GAITRite software. Regardless, use of different technology, for example, accelerometry (Motl et al., 2012; Spain et al., 2012), could offer the means to continuously measure parameters while removing the potential for changes in gait due to the presence of the GAITRite walkway. In summary, the novel results of this investigation indicate that the reduction in walking velocity during the 6MW in individuals with MS who require assistance while walking occurs mainly through a change in the temporal properties of gait. This indirectly suggests that rehabilitation approaches targeting gait timing could result in improvements in 6MW performance. In addition, the marked increase in gait variability in the individuals with MS who require assistance while walking indicates that the control of walking further deteriorates over the course of the 6MW test.
Acknowledgements The authors thank M.K. Boes for assistance with data collection and the staff of the Illinois Simulator Laboratory at the University of Illinois at Urbana-Champaign. Conflicts of interest
There are no conflicts of interest.
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